Intracellular pathways of CD1 antigen presentation

Nature Reviews Immunology

Volumn 3, Issue 1, 2003, Pages 11-22

  Moody, D Branch ^a   Porcelli, Steven A ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1 ANTIGEN; CD1B ANTIGEN; CD1C ANTIGEN; CD1D ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN SUBUNIT; PROTEINASE; T6 ANTIGEN; UNCLASSIFIED DRUG; ISOPROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; CELL SECRETION; CELL SURFACE; CELLULAR DISTRIBUTION; ENDOCYTOSIS; ENDOSOME; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTIGEN PRESENTING CELL; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD1; ENDOSOMES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS;

EID: 0037268145     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri979     Document Type: Review

References (87)

1. Porcelli, S. A. The CD1 family: a third lineage of antigen-presenting molecules. Adv. Immunol. 59, 1-98 (1995).
2. Kawano, T. et al. CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 278, 1626-1629 (1997). Synthetic α-galactosyl ceramides were discovered as the first known antigens for invariant NKT cells. Fine-specificity studies showed that the α-anomeric linkage of the carbohydrate, a modification that is found rarely in mammalian ceramides, is crucial for T-cell activation.
3. Hiromatsu, K. et al. Induction of CD1-restricted immune responses in guinea pigs by immunization with mycobacterial lipid antigens. J. Immunol. 169, 330-339 (2002).
4. - T lymphoyctes to a microbial antigen. Nature 360, 593-597 (1992).
5. Beckman, E. M. et al. CD1c restricts responses of mycobacteria-specific T cells. Evidence for antigen presentation by a second member of the human CD1 family. J. Immunol. 157, 2796-2803 (1996).
6. - αβ T-cell pool. J. Immunol. 162, 366-371 (1999)
7. Spada, F. M., Koezuka, Y. & Porcelli, S. A. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J. Exp. Med. 188, 1529-1534 (1998).
8. Zeng, Z. et al. Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277, 339-345 (1997). The first crystal structure of a CD1 protein shows that mouse CD1d has a large hydrophobic antigen-binding groove that is composed of two pockets, A′ and F′.
9. 2 or phosphatidylinositol. These structures show that the aliphatic hydrocarbon chains of lipids are inserted into the CD1 groove. The human CD1B groove was shown to be larger than that of mouse CD1d, and it is composed of four pockets - A′, C′, F′ and T′. This modular structure shows how CD1B can bind lipids that vary in overall chain length by inserting the lipids into two or more pockets in the groove.
10. Beckman, E. M. et al. Recognition of a lipid antigen by CD1-restricted αβ T cells. Nature 372, 691-694 (1994).
11. Shamshiev, A et al. Presentation of the same glycolipid by different CD1 molecules. J. Exp. Med 195, 1013-1021 (2002).
12. Sieling, P. A. et al. CD1-restricted T-cell recognition of microbial lipoglycan antigens. Science 269, 227-230 (1995).
13. Moody, D. B. et al. Structural requirements for glycolipid antigen recognition by CD1b-restricted T cells. Science 278, 283-286 (1997).
14. Moody, D. B. et al. CD1c-mediated T-cell recognition of isoprenoid glycolipids in Mycobacterium tuberculosis infection. Nature 404, 884-888 (2000).
15. Shamshiev, A et al. Self glycolipids as T-cell autoantigens. Eur. J. Immunol. 29, 1667-1675 (1999). This study provides the first clear functional evidence for the presentation of self-glycolipids by nonendosomal mechanisms.
16. + T-cell antigen receptor α-chain expanded in unprimed mice. Proc. Natl Acad. Sci. USA 87, 5248-5252 (1990).
17. - and heterogeneous with respect to TCRβ expression. Hum. Immunol. 48, 63-67 (1996).
18. Grant, E. P. et al. Molecular recognition of lipid antigens by T-cell receptors. J. Exp. Med. 189, 195-205 (1999).
19. Behar, S. M., Podrebarac, T. A., Roy, C. J., Wang, C. R. & Brenner, M. B. Diverse TCRs recognize murine CD1. J. Immunol. 162, 161-167 (1999).
20. + T cells in major histocompatibility complex class II-deficient mice. J. Exp. Med. 182, 993-1004 (1995).
21. Burdin, N. et al. Structural requirements for antigen presentation by mouse CD1. Proc. Natl Acad. Sci. USA 97, 10156-10161 (2000).
22. Jackman, R. M. et al. The tyrosine-containing cytoplasmic tail of CD1b is essential for its efficient presentation of bacterial lipid antigens. Immunity 8, 341-351 (1998).
23. Chiu, Y. H. et al. Distinct subsets of CD1d-restricted T cells recognize self-antigens loaded in different cellular compartments. J. Exp. Med. 189, 103-110 (1999).
24. Sugita, M. et al. Separate pathways for antigen presentation by CD1 molecules. Immunity 11, 743-752 (1999).
25. Sugita, M., van Der, W., Rogers, R. A., Peters, P. J. & Brenner, M. B. CD1c molecules broadly survey the endocytic system. Proc. Natl Acad. Sci. 97, 8445-8450 (2000).
26. Moody, D. B. et al. Lipid length controls antigen entry into endosomal and nonendosomal pathways for CD1b presentation. Nature Immunol. 3, 435-442 (2002). This study provides direct evidence for the role of alkyl chain length in controlling whether lipids are presented by endosomal or non-endosomal pathways.
27. Chiu, Y. H. et al. Multiple defects in antigen presentation and T-cell development by mice expressing cytoplasmic-tail-truncated CD1d. Nature Immunol. 3, 55-60 (2002).
28. Roberts, T. J. et al. Recycling CD1d1 molecules present endogenous antigens processed in an endocytic compartment to NKT cells. J. Immunol. 168, 5409-5414 (2002).
29. Ernst, W. A. et al. Molecular interaction of CD1b with lipoglycan antigens. Immunity 8, 331-340 (1998).
30. Calabi, F. & Milstein, C. A novel family of human major histocompatibility complex-related genes not mapping to chromosome 6. Nature 323, 540-543 (1986).
31. Woolfson, A. & Milstein, C. Alternative splicing generates secretory isoforms of human CD1. Proc. Natl Acad. Sci. USA 91, 6683-6687 (1994).
32. Angenieux, C. et al. Characterization of CD1e, a third type of CD1 molecule expressed in dendritic cells. J. Biol. Chem. 275, 37757-37764 (2000).
33. Sugita, M., Porcelli, S. A. & Brenner, M. B. Assembly and retention of CD1b heavy chains in the endoplasmic reticulum. J. Immunol. 159, 2358-2365 (1997).
34. Huttinger, R., Staffler, G., Majdic, O. & Stockinger, H. Analysis of the early biogenesis of CD1b: involvement of the chaperones calnexin and calreticulin, the proteasome and β2-microglobulin. Int. Immunol. 11, 1615-1623 (1999).
35. Karadimitris, A. et al. Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc. Natl Acad. Sci. USA 98, 3294-3298 (2001).
36. Altamirano, M. M., Blackburn, J. M., Aguayo, C. & Fersht, A. R. Ligand-independent assembly of recombinant human CD1 by using oxidative refolding chromatography. Proc. Natl Acad. Sci. USA 98, 3288-3293 (2001).
37. Joyce, S, et al. Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 279, 1541-1544 (1998).
38. De Silva, A. D. et al. Lipid-protein interactions: the assembly of CD1d1 with cellular phospholipids occurs in the endoplasmic reticulum. J. Immunol. 188, 723-733 (2002).
39. Gumperz, J. et al. Murine CD1d-restricted T-cell recognition of cellular lipids. Immunity 12, 211-221 (2000).
40. Sugita, M, & Brenner, M. B. An unstable β2-microglobulin: major histocompatibility complex class I heavy chain intermediate dissociates from calnexin and then is stabilized by binding peptide. J. Exp. Med. 180, 2163-2171 (1994).
41. Bauer, A. et al. Analysis of the requirement for β2-microglobulin for expression and formation of human CD1 antigens. Eur. J. Immunol. 21, 1366-1373 (1997).
42. + T lymphocytes. Science 268, 863-865 (1995).
43. Kang, S. J. & Cresswell, P. Regulation of intracellular trafficking of human CD1d by association with MHC class II molecules. EMBO J 21, 1650-1660 (2002). This paper provides evidence for the association of CD1D with MHC class II molecules and for a functional role for MHC class-II-invariant-chain complexes in control of the intracellular trafficking of CD1D.
44. Jayawardena-Wolf, J., Benlagha, K., Chiu, Y. H., Mehr, R. & Bendelac, A CD1d endosomal trafficking is independently regulated by an intrinsic CD1d-encoded tyrosine motif and by the invariant chain. Immunity 15, 897-908 (2001). This study provides evidence for two routes of trafficking of CD1D proteins to late endosomes. CD1D proteins can recycle rapidly from the cell surface to endosomes or they can be delivered to this compartment after association with MHC class-II-invariant-chain complexes.
45. Briken, V., Jackman, R. M., Dasgupta, S., Hoening, S. & Porcelli, S. A. Intracellular trafficking pathway of newly synthesized CD1b molecules. EMBO J. 21, 825-834 (2002). These experiments provide evidence for the physical association of the cytoplasmic tail of CD1B with AP2 and AP3 using surface plasmon-resonance assays. In addition, this report provides evidence for the role of this interaction in the intracellular localization of and antigen-presenting function of CD1B.
46. Sugita, M. et al. Failure of trafficking and antigen presentation by CD1 in AP3-deficient cells. Immunity 16, 697-706 (2002). Using a yeast two-hybrid system, this report provides evidence for the association of CD1B with AP2 and AP3. Human cells deficient in AP3 are shown to have a reduced efficiency of lipid-antigen presentation.
47. Boehm, M. & Bonifacino, J. S. Genetic analyses of adaptin function from yeast to mammals. Gene 286, 176-186 (2002).
48. Kantheti, P. et al. Mutation in AP3δ in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes and synaptic vesicles. Neuron 21, 111-122 (1998).
49. Dell'Angelica, E C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A. & Bonifacino, J. S. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the β3A subunit of the AP3 adaptor. Mol. Cell 3, 11-21 (1999).
50. Owen, D. J. & Evans, P. R. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332 (1998).
51. Ohno, H. et al. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875 (1995).
52. Bonifacino, J. S. & Dell'Angelica, E. C. Molecular bases for the recognition of tyrosine-based sorting signals. J. Cell Biol. 145, 923-926 (1999).
53. Johnson, K. F. & Kornfeld, S. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J. Biol. Chem. 267, 17110-17115 (1992).
54. Letourneur, F. & Klausner, R. D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157 (1992).
55. Rapoport, I., Chen, Y. C., Cupers, P., Shoelson, S. E. & Kirchhausen, T. Dileucine-based sorting signals bind to the β-chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J. 17, 2146-2155 (1998).
56. Rodionov, D. G. & Bakke, O. Medium chains of adaptor complexes AP-1 and AP-2 recognize leucine-based sorting signals from the invariant chain. J. Biol. Chem. 273, 6005-6008 (1998).
57. Greenberg, M., DeTulleo, L., Rapoport, I., Skowronski, J. & Kirchhausen. T. A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr. Biol. 8, 1239-1242 (1998).
58. Salamero, J., Le Borgne, R., Saudrais, C., Goud, B. & Hoflack, B. Expression of major histocompatibility complex class II molecules in HeLa cells promotes the recruitment of AP-1 Golgi-specific assembly proteins on Golgi membranes. J. Biol. Chem. 271, 30318-30321 (1996).
59. Kang, S., Liang, L., Parker, C. D. & Collawn, J. F. Structural requirements for major histocompatibility complex class II invariant chain endocytosis and lysosomal targeting. J. Biol. Chem. 273, 20644-20652 (1998).
60. Zhong, G., Romagnoli, P. & Germain, R. N. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J. Exp. Med. 185, 429-438 (1997).
61. Kongsvik, T. L., Honing, S., Bakke, O. & Rodionov, D. G. Mechanism of interaction between leucine-based sorting signals from the invariant chain and clathrin-associated adaptor protein complexes AP1 and AP2. J. Biol. Chem. 277, 16484-16488 (2002).
62. - cytolytic T lymphocytes. Nature 341, 447-450 (1989).
63. Briken, V., Jackman, R. M., Watts, G. F., Rogers, R. A. & Porcelli, S A. Human CD1b and CD1c isoforms survey different intracellular compartments for the presentation of microbial lipid antigens. J. Exp. Med 192, 281-288 (2000).
64. Sieling. P. A. et al. Human double-negative T cells in systemic lupus erythematosus provide help for IgG and are restricted by CD1c. J. Immunol. 165, 5338-5344 (2000).
65. Moody, D. B. Polyisoprenyl glycolipids as targets of CD1-mediated T-cell responses. Cell Mol. Life Sci. 58, 1461-1474 (2001).
66. Rodionov, D. G., Nordeng, T. W., Pedersen, K., Balk, S. P. & Bakke, O. A critical tyrosine residue in the cytoplasmic tail is important for CD1d internalization but not for its basolateral sorting in MDCK cells. J. Immunol. 162. 1488-1495 (1999).
67. Blumberg, R. S., Colgan, S. P. & Balk, S. P. CD1d: outside-in antigen presentation in the intestinal epithelium? Clin. Exp. Immunol. 109, 223-225 (1997).
68. Rodionov, D. G., Nordeng, T. W., Kongsvik, T. L. & Bakke, O. The cytoplasmic tail of CD1d contains two overlapping basolateral sorting signals. J. Biol. Chem. 275, 8279-8282 (2000).
69. Mellman, I. & Steinman, R. M. Dendritic cells: specialized and regulated antigen-processing machines. Cell 106, 255-258 (2001).
70. Boes, M. et al. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418, 983-988 (2002).
71. + T-cell selection and maturation by cathepsin S. Immunity 15, 909-919 (2001).
72. Honey, K. et al. Thymocyte expression of cathepsin L is essential for NKT-cell development. Nature Immunol. 3, 1069-1074 (2002).
73. Nakagawa, T. Y. & Rudensky, A. Y. The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol. Rev. 172, 121-129 (1999).
74. Sugita, M. et al. Cytoplasmic tail-dependent localization of CD1b antigen-presenting molecules to MIICs. Science 273, 349-352 (1996). This report provides the first evidence that tyrosine-based sequences of CD1 proteins have a role in the delivery of CD1 proteins to late compartments in the endosomal network, including the MHC class II compartment.
75. Moody, D. B., Reinhold, B. B., Reinhold, V. N., Besra, G. S. & Porcelli, S. A. Uptake and processing of glycosylated mycolates for presentation to CD1b-restricted T cells. Immunol. Lett 65, 85-91 (1999).
76. Geho, D. H. et al. Glcosyl-phosphatidylinositol reanchoring unmasks distinct antigen-presenting pathways for CD1b and CD1c. J. Immunol. 165, 1272-1277 (2000).
77. Shamshiev. A. et al. The αβ T-cell response to self-glycolipids shows a novel mechanism of CD1b loading and a requirement for complex oligosaccharides. Immunity 13, 255-264 (2000).
78. Prigozy T. I. et al. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity 6, 187-197 (1997).
79. Brossay, L. et al. Structural requirements for galactosylceramide recognition by CD1-restricted NK T cells. J. Immunol. 161, 5124-5128 (1998).
80. Mukherjee, S., Soe, T. T. & Maxfield, F. R. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol. 144, 1271-1284 (1999).
81. Ferrari, G., Langen, H., Naito, M. & Pieters, J. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97, 435-447 (1999).
82. + T cells of mycobacteria growing in human macrophages. Science 260, 984-986 (1993).
83. Cresswell, P. Invariant chain structure and MHC class II function. Cell 84, 505-507 (1996).
84. Schaible, U. E., Hagens, K., Fischer, K., Collins, H. L. & Kaufmann, S. H. Intersection of group I CD1 molecules and mycobacteria in different intracellular compartments of dendritic cells. J. Immunol. 164, 4843-4852 (2000).
85. Rush, J. S., Sweitzer, T., Kent, C., Decker, G. L. & Waechter, C. J. Biogenesis of the endoplasmic reticulum in activated B lymphocytes: temporal relationships between the induction of protein N-glycosylation activity and the biosynthesis of membrane protein and phospholipid. Arch. Biochem. Biophys. 284, 3-70 (1991).
86. Maccioni, H. J., Daniotti, J. L. & Martina, J. A. Organization of ganglioside synthesis in the Golgi apparatus. Biochim. Biophys. Acta 1437, 101-118 (1999).
87. Melian, A. et al. Molecular recognition of human CD1b antigen complexes: evidence for a common pattern of interaction with αβ TCRs. J. Immunol. 165, 4494-4504 (2000).