Differential alteration of lipid antigen presentation to NKT cells due to imbalances in lipid metabolism

European Journal of Immunology

Volumn 37, Issue 6, 2007, Pages 1431-1441

  Schümann, Jens ^a   Facciotti, Federica ^a   Panza, Luigi ^b   Michieletti, Mario ^b   Compostella, Federica ^c   Collmann, Anthony ^a   Mori, Lucia ^a   De Libero, Gennaro ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Galactosidase; CD1; Niemann Pick C2; NKT cells

Indexed keywords

CD1D ANTIGEN; CD4 ANTIGEN; LIPID; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; GALACTOSIALIDOSIS; IMMUNE DEFICIENCY; LIPID METABOLISM; LIPID STORAGE; LYMPHOCYTE SUBPOPULATION; METABOLIC DISORDER; MOUSE; NATURAL KILLER T CELL; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; THYMOCYTE;

1-DEOXYNOJIRIMYCIN; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD1; ANTIGENS, CD4; BETA-GALACTOSIDASE; DENDRITIC CELLS; ENZYME INHIBITORS; GALACTOSYLCERAMIDES; GLOBOSIDES; GLYCOLIPIDS; HUMANS; LIPID METABOLISM; LIPID METABOLISM DISORDERS; LIVER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL; SPLEEN; T-LYMPHOCYTE SUBSETS; THYMUS GLAND; TRIHEXOSYLCERAMIDES; VESICULAR TRANSPORT PROTEINS;

EID: 34250659321     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200737160     Document Type: Article

References (54)

1. β family. Proc. Natl. Acad. Sci. USA 1992. 89: 6506-6510.
2. + cells in the liver of mice. J. Exp. Med. 1994. 180: 699-704.
3. - T cells in mice and humans. J. Exp. Med. 1994. 180: 1097-1106.
4. + cells in mouse liver. J. Exp. Med. 1996. 183: 1277-1282.
5. Godfrey, D. I. and Kronenberg, M., Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 2004. 114: 1379-1388.
6. Yu, K. O. A. and Porcelli, S. A., The diverse functions of CD1d-restricted NKT cells and their potential for immunotherapy. Immunol. Lett. 2005. 100: 42-55.
7. Gapin, L., Matsuda, J. L., Surh, C. D. and Kronenberg, M., NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2001. 2: 971-978.
8. Dao, T., Gun, D., Ploss, A., Stolzer, A., Saylor, C., Boursalian, T. E., Im, J. S. and Sant'Angelo, D. B., Development of CD1d-restricted NKT cells in the mouse thymus. Eur. J. Immunol. 2004. 34: 3542-3552.
9. + stage of thymic ontogeny. Proc. Natl. Acad. Sci. USA 2005. 102: 5114-5119.
10. Egawa, T., Eberl, G., Taniuchi, I., Benlagha, K., Geissmann, F., Hennighausen, L., Bendelac, A. and Littman, D. R., Genetic evidence supporting selection of the Vα14i NKT cell lineage from double-positive thymocyte precursors. Immunity 2005. 22: 705-716.
11. Benlagha, K., Wei, D. G., Veiga, J., Teyton, L. and Bendelac, A., Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 2005. 202: 485-492.
12. + CD1d-dependent precursor stage. J. Exp. Med. 2002. 195: 835-844.
13. Benlagha, K., Kyin, T., Beavis, A., Teyton, L. and Bendelac, A., A thymic precursor to the NK T cell lineage. Science 2002. 296: 553-555.
14. Gadue, P. and Stein, P. L., NK T cell precursors exhibit differential cytokine regulation and require Itk for efficient maturation. J. Immunol. 2002. 169: 2397-2406.
15. - thymocytes by class I molecules expressed by hematopoietic cells. J. Exp. Med. 1993, 178: 901-908.
16. + thymocytes selected by MHC class I molecules. Science 1994. 263: 1774-1778.
17. Forestier, C., Park, S. H., Wei, D., Berdagha, K., Teyton, L. and Bendelac, A., T cell development in mice expressing CD1d directed by a classical MHC class II promoter. J. Immunol. 2003. 171: 4096-4104.
18. + T cells. J. Immunol. 2003. 171: 4105-4112.
19. + cells. J. Immunol. 2000. 164: 2412-2418.
20. + T cells by CD1-expressing cortical thymocytes. J. Exp. Med. 1995. 182: 2091-2096.
21. Wei, D. G., Lee, H., Park, S. H., Beaudoin, L., Teyton, L., Lehuen, A. and Bendelac, A., Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J. Exp. Med., 2005. 202: 239-248.
22. Schümann, J., Pittoni, P., Tonti, E., MacDonald, H. R., Dellabona, P. and Casorati, G., Targeted expression of human CD1d in transgenic mice reveals independent roles for thymocytes and thymic antigen-presenting cells in positive and negative selection of Vα14i NKT cells. J. Immunol. 2005. 175: 7303-7310.
23. Chun, T., Page, M. J., Gapin, L., Matsuda, J. L., Xu, H., Nguyen, H., Kang, H. S. et al., CD1d-expressing dendritic cells but not thymic epithelial cells can mediate negative selection of NKT cells. J. Exp. Med. 2003. 197: 907-918.
24. De Libero, G. and Mori, L., Mechanisms of lipid-antigen generation and presentation to T cells. Trends Immunol. 2006. 27: 485-492.
25. Savage, P. B., Teyton, L. and Bendelac, A., Glycolipids for natural killer T cells. Chem. Soc. Rev. 2006. 35: 771-779.
26. Sullivan, B. A., Nagarajan, N. A. and Kronenberg, M., CD1 and MHC II find different means to the same end. Trends Immunol. 2005. 26: 282-288.
27. Hava, D. L., Brigl, M., Van den Elzen, P., Zajonc, D. M., Wilson, I. A. and Brenner, M. B., CD1 assembly and the formation of CD1-antigen complexes. Curr. Opin. Immunol. 2005. 17: 88-94.
28. Zhou, D., Mattner, J., Cantu, C. III, Schrantz, N., Yin, N., Gao, Y., Sagiv, Y. et al., Lysosomal glycosphingolipid recognition by NKT cells. Science 2004. 306: 1786-1789.
29. Zhou, D., Cantu, C. III, Sagiv, Y., Schrantz, N., Kulkarni, A. B., Qi, X., Mahuran, D. J. et al., Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 2004. 303: 523-527.
30. Kang, S. J. and Cresswell, P., Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat. Immunol. 2004. 5: 175-181.
31. Sagiv, Y., Hudspeth, K., Mattner, J., Schrantz, N., Stern, R. K., Zhou, D., Savage, P. B. et al., Cutting edge: Impaired glycosphingolipid trafficking and NKT cell development in mice lacking Niemann-Pick type C1 protein. J. Immunol. 2006. 177: 26-30.
32. Gadola, S. D., Silk, J. D., Jeans, A., Illarionov, P. A., Salio, M., Besra, G. S., Dwek, R. et al., Impaired selection of invariant natural killer T cells in diverse mouse models of glycosphingolipid lysosomal storage diseases. J. Exp. Med. 2006. 203: 2293-2303.
33. Schümann, J., Voyle, R. B., Wei, B. Y. and MacDonald, H. R., Cutting edge: Influence of the TCR Vβ domain on the avidity of CD1d:α-galactosylcer-galactosylceramide binding by invariant Vα14 NKT cells. J. Immunol. 2003. 170: 5815-5819.
34. Stanic, A. K., Shashidharamurthy, R., Bezbradica, J. S., Matsuki, N., Yoshimura, Y., Miyake, S., Choi, E. Y. et al., Another view of T cell antigen recognition: cooperative engagement of glycolipid antigens by Vα14Jα18 natural T (iNKT) cell receptor. J. Immunol. 2003. 171: 4539-4551.
35. Schümann, J., Mycko, M. P., Dellabona, P., Casorati, G. and MacDonald, H. R., Cutting edge: Influence of the TCR Vβ domain on the selection of semi-invariant NKT cells by endogenous ligands. J. Immunol. 2006. 176: 2064-2068.
36. Wei, D. G., Curran, S. A., Savage, P. B., Teyton, L. and Bendelac, A., Mechanisms imposing the Vβ bias of Vα14 natural killer T cells and consequences for microbial glycolipid recognition. J. Exp. Med. 2006. 203: 1197-1207.
37. Kofter, T. and Sandhoff, K., Principles of lysosomal membrane digestion: Stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell. Dev. Biol. 2005. 21: 81-103.
38. Platt, F. M. and Butters, T. D., New therapeutic prospects for the glycosphingolipid lysosomal storage diseases. Biochem. Pharmacol. 1998. 56: 421-430.
39. Yu, K. O. A., Im, J. S., Molano, A., Dutronc, Y., Illarionov, P. A., Forestier, C., Fujiwara, N. et al., Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of α-galactosylceramides. Proc. Natl. Acad. Sci. USA 2005. 102: 3383-3388.
40. Sleat, D. E., Wiseman, J. A., El-Banna, M., Price, S. M., Verot, L., Shen, M. M., Tint, G. S. et al., Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl. Acad. Sci. USA 2004. 101: 5886-5891.
41. Mukherjee, S. and Maxfield, F. R., Lipid and cholesterol trafficking in NPC. Biochim. Biophys. Acta 2004. 1685: 28-37.
42. Cheruku, S. R., Xu, Z., Dutia, R., Lobel, P. and Storch, J., Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J. Biol. Chem. 2006. 281: 31594-31604.
43. Zajonc, D. M., Cantu, C. III, Mattner, J., Zhou, D., Savage, P. B., Bendelac, A., Wilson, I. A. and Teyton, L., Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat. Immunol. 2005. 6: 810-818.
44. Matsuda, J., Suzuki, O., Oshima, A., Ogura, A., Naiki, M. and Suzuki, Y., Neurological manifestations of knockout mice with β-galactosidase deficiency. Brain Dev. 1997. 19: 19-20.
45. M1-gangliosidosis. Glycoconj. J. 1997. 14: 729-736.
46. M1-ganglioside accumulation in mice defective in lysosomal acid β-galactosidase. Hum. Mol. Genet. 1997 6: 205-211.
47. Zschoche, A., Fürst, W., Schwarzmann, G. and Sandhoff, K., Hydrolysis of lactosylceramide by human galactosylceramidase and GM1-β-galactosidase in a detergent-free system and its stimulation by sphingolipid activator proteins, sap-B and sap-C. Eur. J. Biochem. 1994. 222: 83-90.
48. Tohyama, J., Vanier, M. T., Suzuki, K., Ezoe, T., Matsuda, J. and Suzuki, K., Paradoxical influence of acid β-galactosidase gene dosage on phenotype of the twitcher mouse (genetic galactosylceramidase deficiency). Hum. Mol. Genet. 2000. 9: 1699-1707.
49. Naidenko, O. V., Maher, J. K., Ernst, W. A., Sakai, T., Modlin, R. L. and Kronenberg, M., Binding and antigen presentation of ceramide-containing glycolipids by soluble mouse and human CD1d molecules. J. Exp. Med. 1999. 190: 1069-1079.
50. Stanic, A. K., De Silva, A. D., Park, J. J., Sriram, V., Ichikawa, S., Hirabyashi, Y., Hayakawa, K. et al., Defective presentation of the CD1d1-restricted Va14Ja18 NKT lymphocyte antigen caused by β-d-glucosylceramide synthase deficiency. Proc. Natl. Acad. Sci. USA 2003. 100: 1849-1854.
51. + thymocytes. J. Immunol. 1993. 151: 1868-1880.
52. Schmidt, R. R. and Maier, T., Synthesis of d-ribo- and 1-lyxo-phytosphingosine: transformation into the corresponding lactosyl-ceramides. Carbohy. Res. 1988. 174: 169-179.
53. Wessel, H.-P. and Bundle, D. R., Strategies for the synthesis of branched oligosaccharides of the Shigella flexneri 5a, 5b, and variant X serogroups employing a multifunctional rhamnose precursor. J. Chem. Soc. Perkin Trans. 19851, 2251-2260.
54. Murata, K., Toba, T., Nakanishi, K., Takahashi, B., Yamamura, T., Miyake, S. and Annoura, H., Total Synthesis of an Immunosuppressive Glycolipid,