Endoplasmic reticulum glycoprotein quality control regulates CD1d assembly and CD1d-mediated antigen presentation

Journal of Biological Chemistry

Volumn 288, Issue 23, 2013, Pages 16391-16402

  Kunte, Amit ^a   Zhang, Wei ^a   Paduraru, Crina ^a   Veerapen, Natacha ^b   Cox, Liam R ^b   Besra, Gurdyal S ^b   Cresswell, Peter ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNE RESPONSE; ANTIGEN PRESENTATION; ANTIGENICITY; CELL SURFACES; ENDOPLASMIC RETICULUM; GLUCOSYLTRANSFERASES; HIGH AFFINITY; MAJOR HISTOCOMPATIBILITY COMPLEX;

ANTIGENS; CELL MEMBRANES; CYTOLOGY; GLYCOPROTEINS; MACHINERY; QUALITY CONTROL;

QUALITY ASSURANCE;

BETA 2 MICROGLOBULIN; CD1D ANTIGEN; GLUCOSYLTRANSFERASE; UDP GLUCOSE GLYCOPROTEIN GLUCOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGENICITY; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN STABILITY;

ANTIGEN PROCESSING; ER QUALITY CONTROL; MAJOR HISTOCOMPATIBILITY COMPLEX (MHC); T CELL; TRANSPORT;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD1D; BETA 2-MICROGLOBULIN; CELL LINE; ENDOPLASMIC RETICULUM; GLUCOSYLTRANSFERASES; MICE; MICE, MUTANT STRAINS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN TRANSPORT;

EID: 84878750391     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.474221     Document Type: Article

References (51)

1. De Libero, G., and Mori, L. (2012) Novel insights into lipid antigen presentation. Trends Immunol. 33, 103-111
2. Porcelli, S. A., and Modlin, R. L. (1999) The CD1 system. Antigen-presenting molecules for T cell recognition of lipids and glycolipids. Annu. Rev. Immunol. 17, 297-329 (Pubitemid 29241127)
3. Bendelac, A., Savage, P. B., and Teyton, L. (2007) The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (Pubitemid 46697911)
4. Berzins, S. P., Smyth, M. J., and Baxter, A. G. (2011) Presumed guilty. Natural killer T cell defects and human disease. Nat. Rev. Immunol. 11, 131-142
5. Godfrey, D. I., MacDonald, H. R., Kronenberg, M., Smyth, M. J., and Van Kaer, L. (2004) NKT cells. what's in a name? Nat. Rev. Immunol. 4, 231-237
6. Tupin, E., Kinjo, Y., and Kronenberg, M. (2007) The unique role of natural killer T cells in the response to microorganisms. Nat. Rev. Microbiol. 5, 405-417 (Pubitemid 46780078)
7. Brigl, M., and Brenner, M. B. (2010) How invariant natural killer T cells respond to infection by recognizing microbial or endogenous lipid antigens. Semin. Immunol. 22, 79-86
8. Terabe, M., and Berzofsky, J. A. (2008) The role of NKT cells in tumor immunity. Adv. Cancer Res. 101, 277-348
9. Mallevaey, T., and Selvanantham, T. (2012) Strategy of lipid recognition by invariant natural killer T cells. "One for all and all for one." Immunology 136, 273-282
10. Rossjohn, J., Pellicci, D. G., Patel, O., Gapin, L., and Godfrey, D. I. (2012) Recognition of CD1d-restricted antigens by natural killer T cells. Nat. Rev. Immunol. 12, 845-857
11. Joyce, S., Girardi, E., and Zajonc, D. M. (2011) NKT cell ligand recognition logic. Molecular basis for a synaptic duet and transmission of inflammatory effectors. J. Immunol. 187, 1081-1089
12. McCarthy, C., Shepherd, D., Fleire, S., Stronge, V. S., Koch, M., Illarionov, P. A., Bossi, G., Salio, M., Denkberg, G., Reddington, F., Tarlton, A., Reddy, B. G., Schmidt, R. R., Reiter, Y., Griffiths, G. M., van der Merwe, P. A., Besra, G. S., Jones, E. Y., Batista, F. D., and Cerundolo, V. (2007) The length of lipids bound to human CD1d molecules modulates the affinity of NKT cell TCR and the threshold of NKT cell activation. J. Exp. Med. 204, 1131-1144 (Pubitemid 46798156)
13. Im, J. S., Arora, P., Bricard, G., Molano, A., Venkataswamy, M. M., Baine, I., Jerud, E. S., Goldberg, M. F., Baena, A., Yu, K. O., Ndonye, R. M., Howell, A. R., Yuan, W., Cresswell, P., Chang, Y. T., Illarionov, P. A., Besra, G. S., and Porcelli, S. A. (2009) Kinetics and cellular site of glycolipid loading control the outcome of natural killer T cell activation. Immunity 30, 888-898
14. Koch, M., Stronge, V. S., Shepherd, D., Gadola, S. D., Mathew, B., Ritter, G., Fersht, A. R., Besra, G. S., Schmidt, R. R., Jones, E. Y., and Cerundolo, V. (2005) The crystal structure of human CD1d with and without α-galactosylceramide. Nat. Immunol. 6, 819-826 (Pubitemid 43090468)
15. Hayakawa, Y., Takeda, K., Yagita, H., Van Kaer, L., Saiki, I., and Okumura, K. (2001) Differential regulation of Th1 and Th2 functions of NKT cells by CD28 and CD40 costimulatory pathways. J. Immunol. 166, 6012-6018 (Pubitemid 32440726)
16. Kang, S. J., and Cresswell, P. (2002) Calnexin, calreticulin, and ERp57 cooperate in disulfide bond formation in human CD1d heavy chain. J. Biol. Chem. 277, 44838-44844
17. Brozovic, S., Nagaishi, T., Yoshida, M., Betz, S., Salas, A., Chen, D., Kaser, A., Glickman, J., Kuo, T., Little, A., Morrison, J., Corazza, N., Kim, J. Y., Colgan, S. P., Young, S. G., Exley, M., and Blumberg, R. S. (2004) CD1d function is regulated by microsomal triglyceride transfer protein. Nat. Med. 10, 535-539 (Pubitemid 38667914)
18. Dougan, S. K., Rava, P., Hussain, M. M., and Blumberg, R. S. (2007) MTP regulated by an alternate promoter is essential for NKT cell development. J. Exp. Med. 204, 533-545 (Pubitemid 46457077)
19. Dougan, S. K., Salas, A., Rava, P., Agyemang, A., Kaser, A., Morrison, J., Khurana, A., Kronenberg, M., Johnson, C., Exley, M., Hussain, M. M., and Blumberg, R. S. (2005) Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells. J. Exp. Med. 202, 529-539 (Pubitemid 41186951)
20. Park, J. J., Kang, S. J., De Silva, A. D., Stanic, A. K., Casorati, G., Hachey, D. L., Cresswell, P., and Joyce, S. (2004) Lipid-protein interactions. Biosynthetic assembly of CD1 with lipids in the endoplasmic reticulum is evolutionarily conserved. Proc. Natl. Acad. Sci. U.S.A. 101, 1022-1026 (Pubitemid 38160577)
21. Yuan, W., Kang, S. J., Evans, J. E., and Cresswell, P. (2009) Natural lipid ligands associated with human CD1d targeted to different subcellular compartments. J. Immunol. 182, 4784-4791
22. Salio, M., Silk, J. D., and Cerundolo, V. (2010) Recent advances in processing and presentation of CD1 bound lipid antigens. Curr. Opin. Immunol. 22, 81-88
23. Zeissig, S., Murata, K., Sweet, L., Publicover, J., Hu, Z., Kaser, A., Bosse, E., Iqbal, J., Hussain, M. M., Balschun, K., Röcken, C., Arlt, A., Günther, R., Hampe, J., Schreiber, S., Baron, J. L., Moody, D. B., Liang, T. J., and Blumberg, R. S. (2012) Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat. Med. 18, 1060-1068
24. Zhu, Y., Zhang, W., Veerapen, N., Besra, G., and Cresswell, P. (2010) Calreticulin controls the rate of assembly of CD1d molecules in the endoplasmic reticulum. J. Biol. Chem. 285, 38283-38292
25. Dejgaard, S., Nicolay, J., Taheri, M., Thomas, D. Y., and Bergeron, J. J. (2004) The ER glycoprotein quality control system. Curr. Issues Mol. Biol. 6, 29-42 (Pubitemid 37441572)
26. Tamura, T., Sunryd, J. C., and Hebert, D. N. (2010) Sorting things out through endoplasmic reticulum quality control. Mol. Membr. Biol. 27, 412-427
27. Caramelo, J. J., Castro, O. A., Alonso, L. G., De Prat-Gay, G., and Parodi, A. J. (2003) UDP-Glc:glycoprotein glucosyltransferase recognizes structured and solvent-accessible hydrophobic patches in molten globule-like folding intermediates. Proc. Natl. Acad. Sci. U.S.A. 100, 86-91 (Pubitemid 36078034)
28. Caramelo, J. J., Castro, O. A., de Prat-Gay, G., and Parodi, A. J. (2004) The endoplasmic reticulum glucosyltransferase recognizes nearly native glycoprotein folding intermediates. J. Biol. Chem. 279, 46280-46285 (Pubitemid 39491623)
29. Ritter, C., Quirin, K., Kowarik, M., and Helenius, A. (2005) Minor folding defects trigger local modification of glycoproteins by the ER folding sensor GT. EMBO J. 24, 1730-1738 (Pubitemid 40704983)
30. Molinari, M. (2007) N-Glycan structure dictates extension of protein folding or onset of disposal. Nat. Chem. Biol. 3, 313-320
31. Wearsch, P. A., Peaper, D. R., and Cresswell, P. (2011) Essential glycandependent interactions optimize MHC class I peptide loading. Proc. Natl. Acad. Sci. U.S.A. 108, 4950-4955
32. Zhang, W., Wearsch, P. A., Zhu, Y., Leonhardt, R. M., and Cresswell, P. (2011) A role for UDP-glucose glycoprotein glucosyltransferase in expression and quality control of MHC class I molecules. Proc. Natl. Acad. Sci. U.S.A. 108, 4956-4961
33. Soldà, T., Galli, C., Kaufman, R. J., and Molinari, M. (2007) Substrate-specific requirements for UGT1-dependent release from calnexin. Molecular cell 27, 238-249 (Pubitemid 47058298)
34. Florence, W. C., Xia, C., Gordy, L. E., Chen, W., Zhang, Y., Scott-Browne, J., Kinjo, Y., Yu, K. O., Keshipeddy, S., Pellicci, D. G., Patel, O., Kjer-Nielsen, L., McCluskey, J., Godfrey, D. I., Rossjohn, J., Richardson, S. K., Porcelli, S. A., Howell, A. R., Hayakawa, K., Gapin, L., Zajonc, D. M., Wang, P. G., and Joyce, S. (2009) Adaptability of the semi-invariant natural killer T-cell receptor towards structurally diverse CD1d-restricted ligands. EMBO J. 28, 3579-3590
35. Gui, M., Li, J., Wen, L. J., Hardy, R. R., and Hayakawa, K. (2001) TCRβ chain influences but does not solely control autoreactivity of Vα14J281T cells. J. Immunol. 167, 6239-6246 (Pubitemid 33081553)
36. Bendelac, A., Lantz, O., Quimby, M. E., Yewdell, J. W., Bennink, J. R., and Brutkiewicz, R. R. (1995) CD1 recognition by mouse NK1+ T lymphocytes. Science 268, 863-865
37. Somnay-Wadgaonkar, K., Nusrat, A., Kim, H. S., Canchis, W. P., Balk, S. P., Colgan, S. P., and Blumberg, R. S. (1999) Immunolocalization of CD1d in human intestinal epithelial cells and identification of a β2-microglobulin- associated form. Int. Immunol. 11, 383-392 (Pubitemid 29121625)
38. Paduraru, C., Spiridon, L., Yuan, W., Bricard, G., Valencia, X., Porcelli, S. A., Illarionov, P. A., Besra, G. S., Petrescu, S. M., Petrescu, A. J., and Cresswell, P. (2006) An N-linked glycan modulates the interaction between the CD1d heavy chain and β2-microglobulin. J. Biol. Chem. 281, 40369-40378 (Pubitemid 46041840)
39. Burdin, N., Brossay, L., Koezuka, Y., Smiley, S. T., Grusby, M. J., Gui, M., Taniguchi, M., Hayakawa, K., and Kronenberg, M. (1998) Selective ability of mouse CD1 to present glycolipids. α-Galactosylceramide specifically stimulates Vα14+ NK T lymphocytes. J. Immunol. 161, 3271-3281
40. Kang, S. J., and Cresswell, P. (2004) Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat. Immunol. 5, 175-181
41. Prigozy, T. I., Naidenko, O., Qasba, P., Elewaut, D., Brossay, L., Khurana, A., Natori, T., Koezuka, Y., Kulkarni, A., and Kronenberg, M. (2001) Glycolipid antigen processing for presentation by CD1d molecules. Science 291, 664-667 (Pubitemid 32150427)
42. Yu, K. O., Im, J. S., Molano, A., Dutronc, Y., Illarionov, P. A., Forestier, C., Fujiwara, N., Arias, I., Miyake, S., Yamamura, T., Chang, Y. T., Besra, G. S., and Porcelli, S. A. (2005) Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of α-galactosylceramides. Proc. Natl. Acad. Sci. U.S.A. 102, 3383-3388 (Pubitemid 40328054)
43. Pearse, B. R., Tamura, T., Sunryd, J. C., Grabowski, G. A., Kaufman, R. J., and Hebert, D. N. (2010) The role of UDP-Glc:glycoprotein glucosyltransferase 1 in the maturation of an obligate substrate prosaposin. J. Cell Biol. 189, 829-841
44. Zhou, D., Cantu, C., 3rd, Sagiv, Y., Schrantz, N., Kulkarni, A. B., Qi, X., Mahuran, D. J., Morales, C. R., Grabowski, G. A., Benlagha, K., Savage, P., Bendelac, A., and Teyton, L. (2004) Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 303, 523-527 (Pubitemid 38120850)
45. Springer, S., Doring, K., Skipper, J. C., Townsend, A. R., and Cerundolo, V. (1998) Fast association rates suggest a conformational change in the MHC class I molecule H-2Db upon peptide binding. Biochemistry 37, 3001-3012 (Pubitemid 28145753)
46. van der Burg, S. H., Visseren, M. J., Brandt, R. M., Kast, W. M., and Melief, C. J. (1996) Immunogenicity of peptides bound to MHC class I molecules depends on the MHC-peptide complex stability. J. Immunol. 156, 3308-3314 (Pubitemid 26123546)
47. Cerundolo, V., Elliott, T., Elvin, J., Bastin, J., Rammensee, H. G., and Townsend, A. (1991) The binding affinity and dissociation rates of peptides for class I major histocompatibility complex molecules. Eur. J. Immunol. 21, 2069-2075
48. Odyniec, A. N., Barral, D. C., Garg, S., Tatituri, R. V., Besra, G. S., and Brenner, M. B. (2010) Regulation of CD1 antigen-presenting complex stability. J. Biol. Chem. 285, 11937-11947
49. Sagiv, Y., Bai, L., Wei, D. G., Agami, R., Savage, P. B., Teyton, L., and Bendelac, A. (2007) A distal effect of microsomal triglyceride transfer protein deficiency on the lysosomal recycling of CD1d. J. Exp. Med. 204, 921-928 (Pubitemid 46631619)
50. Sriram, V., Willard, C. A., Liu, J., and Brutkiewicz, R. R. (2008) Importance of N-linked glycosylation in the functional expression of murine CD1d1. Immunology 123, 272-281
51. Brennan, P. J., Tatituri, R. V., Brigl, M., Kim, E. Y., Tuli, A., Sanderson, J. P., Gadola, S. D., Hsu, F. F., Besra, G. S., and Brenner, M. B. (2011) Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat. Immunol. 12, 1202-1211