The CD1 size problem: Lipid antigens, ligands, and scaffolds

Cellular and Molecular Life Sciences

Volumn 71, Issue 16, 2014, Pages 3069-3079

  Ly, Dalam ^a   Moody, D Branch ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

CD1; Lipid antigens; Scaffolds; Spacers; Structures

Indexed keywords

CD1 ANTIGEN; CD1B ANTIGEN; CD1C ANTIGEN; CD1D ANTIGEN; CD1E ANTIGEN; SCAFFOLD PROTEIN; T6 ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN BINDING; CELL FUNCTION; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; HUMAN; IMMUNOREACTIVITY; IMMUNOREGULATION; LIGAND BINDING; LIPID ANALYSIS; LYMPHOCYTE FUNCTION; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE;

BACTERIA (MICROORGANISMS);

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; ANTIGENS, CD1; HUMANS; LIGANDS; LIPIDS; MODELS, MOLECULAR; PROTEIN CONFORMATION; T-LYMPHOCYTES;

EID: 84905104073     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1603-6     Document Type: Review

References (87)

1. Porcelli S, Brenner MB, Greenstein JL, Balk SP, Terhorst C, Bleicher PA (1989) Recognition of cluster of differentiation 1 antigens by human CD4-CD8-cytolytic T lymphocytes. Nature 341(6241):447-450
2. Porcelli S, Morita CT, Brenner MB (1992) CD1b restricts the response of human CD4-8-T lymphocytes to a microbial antigen. Nature 360(6404):593-597
3. Beckman EM, Porcelli SA, Morita CT, Behar SM, Furlong ST, Brenner MB (1994) Recognition of a lipid antigen by CD1-restricted alpha beta + T cells. Nature 372(6507):691-694
4. Beckman EM, Melian A, Behar SM, Sieling PA, Chatterjee D, Furlong ST, Matsumoto R, Rosat JP, Modlin RL, Porcelli SA (1996) CD1c restricts responses of mycobacteria-specific T cells. evidence for antigen presentation by a second member of the human CD1 family. J Immunol 157(7):2795-2803
5. Borg NA, Wun KS, Kjer-Nielsen L, Wilce MC, Pellicci DG, Koh R, Besra GS, Bharadwaj M, Godfrey DI, McCluskey J, Rossjohn J (2007) CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature 448(7149):44-49
6. Girardi E, Maricic I, Wang J, Mac TT, Iyer P, Kumar V, Zajonc DM (2012) Type II natural killer T cells use features of both innate-like and conventional T cells to recognize sulfatide self antigens. Nat Immunol 13(9):851-856
7. Lopez-Sagaseta J, Kung JE, Savage PB, Gumperz J, Adams EJ (2012) The molecular basis for recognition of CD1d/alpha-galactosylceramide by a human non-valpha24 T cell receptor. PLoS Biol 10(10):e1001412
8. Lopez-Sagaseta J, Sibener LV, Kung JE, Gumperz J, Adams EJ (2012) Lysophospholipid presentation by CD1d and recognition by a human natural killer T-cell receptor. EMBO J 31(8):2047-2059
9. Mallevaey T, Clarke AJ, Scott-Browne JP, Young MH, Roisman LC, Pellicci DG, Patel O, Vivian JP, Matsuda JL, McCluskey J, Godfrey DI, Marrack P, Rossjohn J, Gapin L (2011) A molecular basis for NKT cell recognition of CD1d-self-antigen. Immunity 34(3):315-326
10. Patel O, Pellicci DG, Gras S, Sandoval-Romero ML, Uldrich AP, Mallevaey T, Clarke AJ, Le Nours J, Theodossis A, Cardell SL, Gapin L, Godfrey DI, Rossjohn J (2012) Recognition of CD1d-sulfatide mediated by a type II natural killer T cell antigen receptor. Nat Immunol 13(9):857-863
11. Pellicci DG, Clarke AJ, Patel O, Mallevaey T, Beddoe T, Le Nours J, Uldrich AP, McCluskey J, Besra GS, Porcelli SA, Gapin L, Godfrey DI, Rossjohn J (2011) Recognition of beta-linked self glycolipids mediated by natural killer T cell antigen receptors. Nat Immunol 12(9):827-833
12. Wun KS, Cameron G, Patel O, Pang SS, Pellicci DG, Sullivan LC, Keshipeddy S, Young MH, Uldrich AP, Thakur MS, Richardson SK, Howell AR, Illarionov PA, Brooks AG, Besra GS, McCluskey J, Gapin L, Porcelli SA, Godfrey DI, Rossjohn J (2011) A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Immunity 34(3):327-339
13. Li Y, Girardi E, Wang J, Yu ED, Painter GF, Kronenberg M, Zajonc DM (2010) The valpha14 invariant natural killer T cell TCR forces microbial glycolipids and CD1d into a conserved binding mode. J Exp Med 207(11):2383-2393
14. Girardi E, Yu ED, Li Y, Tarumoto N, Pei B, Wang J, Illarionov P, Kinjo Y, Kronenberg M, Zajonc DM (2011) Unique interplay between sugar and lipid in determining the antigenic potency of bacterial antigens for NKT cells. PLoS Biol 9(11):e1001189
15. Cheng TY, Relloso M, Van Rhijn I, Young DC, Besra GS, Briken V, Zajonc DM, Wilson IA, Porcelli S, Moody DB (2006) Role of lipid trimming and CD1 groove size in cellular antigen presentation. EMBO J 25(13):2989-2999
16. Zeng Z, Castano AR, Segelke BW, Stura EA, Peterson PA, Wilson IA (1997) Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277(5324):339-345
17. Moody DB, Zajonc DM, Wilson IA (2005) Anatomy of CD1-lipid antigen complexes. Nat Rev Immunol 5(5):387-399
18. Gadola SD, Zaccai NR, Harlos K, Shepherd D, Castro-Palomino JC, Ritter G, Schmidt RR, Jones EY, Cerundolo V (2002) Structure of human CD1b with bound ligands at 2.3 A, A maze for alkyl chains. Nat Immunol 3(8):721-726
19. Zajonc DM, Elsliger MA, Teyton L, Wilson IA (2003) Crystal structure of CD1a in complex with a sulfatide self antigen at a resolution of 2.15 A. Nat Immunol 4(8):808-815
20. Scharf L, Li NS, Hawk AJ, Garzon D, Zhang T, Fox LM, Kazen AR, Shah S, Haddadian EJ, Gumperz JE, Saghatelian A, Faraldo-Gomez JD, Meredith SC, Piccirilli JA, Adams EJ (2010) The 2.5-Å structure of CD1c in complex with a mycobacterial lipid reveals an open groove ideally suited for diverse antigen presentation. Immunity 33(6):853-862
21. Garcia-Alles LF, Giacometti G, Versluis C, Maveyraud L, De Paepe D, Guiard J, Tranier S, Gilleron M, Prandi J, Hanau D, Heck AJ, Mori L, De Libero G, Puzo G, Mourey L, De la Salle H (2011) Crystal structure of human CD1e reveals a groove suited for lipid-exchange processes. Proc Natl Acad Sci USA 108(32):13230-13235
22. Zajonc DM, Crispin MD, Bowden TA, Young DC, Cheng TY, Hu J, Costello CE, Rudd PM, Dwek RA, Miller MJ, Brenner MB, Moody DB, Wilson IA (2005) Molecular mechanism of lipopeptide presentation by CD1a. Immunity 22(2):209-219
23. Moody DB, Young DC, Cheng TY, Rosat JP, Roura-Mir C, O'Connor PB, Zajonc DM, Walz A, Miller MJ, Levery SB, Wilson IA, Costello CE, Brenner MB (2004) T cell activation by lipopeptide antigens. Science 303(5657):527-531
24. Batuwangala T, Shepherd D, Gadola SD, Gibson KJ, Zaccai NR, Fersht AR, Besra GS, Cerundolo V, Jones EY (2004) The crystal structure of human CD1b with a bound bacterial glycolipid. J Immunol 172(4):2382-2388
25. Garcia-Alles LF, Collmann A, Versluis C, Lindner B, Guiard J, Maveyraud L, Huc E, Im JS, Sansano S, Brando T, Julien S, Prandi J, Gilleron M, Porcelli SA, De la Salle H, Heck AJ, Mori L, Puzo G, Mourey L, De Libero G (2011) Structural reorganization of the antigen-binding groove of human CD1b for presentation of mycobacterial sulfoglycolipids. Proc Natl Acad Sci USA 108(43):17755-17760
26. Garcia-Alles LF, Versluis K, Maveyraud L, Vallina AT, Sansano S, Bello NF, Gober HJ, Guillet V, De la Salle H, Puzo G, Mori L, Heck AJ, De Libero G, Mourey L (2006) Endogenous phosphatidylcholine and a long spacer ligand stabilize the lipid-binding groove of CD1b. EMBO J 25(15):3684-3692
27. Layre E, Collmann A, Bastian M, Mariotti S, Czaplicki J, Prandi J, Mori L, Stenger S, De Libero G, Puzo G, Gilleron M (2009) Mycolic acids constitute a scaffold for mycobacterial lipid antigens stimulating CD1-restricted T cells. Chem Biol 16(1):82-92
28. Moody DB, Reinhold BB, Guy MR, Beckman EM, Frederique DE, Furlong ST, Ye S, Reinhold VN, Sieling PA, Modlin RL, Besra GS, Porcelli SA (1997) Structural requirements for glycolipid antigen recognition by CD1b-restricted T cells. Science 278(5336):283-286
29. Moody DB, Ulrichs T, Muhlecker W, Young DC, Gurcha SS, Grant E, Rosat JP, Brenner MB, Costello CE, Besra GS, Porcelli SA (2000) CD1c-mediated T-cell recognition of isoprenoid glycolipids in Mycobacterium tuberculosis infection. Nature 404(6780):884-888
30. Ly D, Kasmar AG, Cheng TY, De Jong A, Huang S, Roy S, Bhatt A, van Summeren RP, Altman JD, Jacobs WR JR, Adams EJ, Minnaard AJ, Porcelli SA, Moody DB (2013) CD1c tetramers detect ex vivo T cell responses to processed phosphomycoketide antigens. J Exp Med 210(4):729-741
31. Van Rhijn I, Young DC, De Jong A, Vazquez J, Cheng TY, Talekar R, Barral DC, Leon L, Brenner MB, Katz JT, Riese R, Ruprecht RM, O'Connor PB, Costello CE, Porcelli SA, Briken V, Moody DB (2009) CD1c bypasses lysosomes to present a lipopeptide antigen with 12 amino acids. J Exp Med 206(6):1409-1422
32. Adams EJ (2013) Diverse antigen presentation by the Group 1 CD1 molecule, CD1c. Mol Immunol 55(2):182-185
33. Kinjo Y, Illarionov P, Vela JL, Pei B, Girardi E, Li X, Li Y, Imamura M, Kaneko Y, Okawara A, Miyazaki Y, Gomez-Velasco A, Rogers P, Dahesh S, Uchiyama S, Khurana A, Kawahara K, Yesilkaya H, Andrew PW, Wong CH, Kawakami K, Nizet V, Besra GS, Tsuji M, Zajonc DM, Kronenberg M (2011) Invariant natural killer T cells recognize glycolipids from pathogenic Gram-positive bacteria. Nat Immunol 12(10):966-974
34. Wang J, Li Y, Kinjo Y, Mac TT, Gibson D, Painter GF, Kronenberg M, Zajonc DM (2010) Lipid binding orientation within CD1d affects recognition of Borrelia burgdorferi antigens by NKT cells. Proc Natl Acad Sci USA 107(4):1535-1540
35. Joyce S, Girardi E, Zajonc DM (2011) NKT cell ligand recognition logic: molecular basis for a synaptic duet and transmission of inflammatory effectors. J Immunol 187(3):1081-1089
36. Rossjohn J, Pellicci DG, Patel O, Gapin L, Godfrey DI (2012) Recognition of CD1d-restricted antigens by natural killer T cells. Nat Rev Immunol 12(12):845-857
37. Brennan PJ, Brigl M, Brenner MB (2013) Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 13(2):101-117
38. De la Salle H, Mariotti S, Angenieux C, Gilleron M, Garcia-Alles LF, Malm D, Berg T, Paoletti S, Maitre B, Mourey L, Salamero J, Cazenave JP, Hanau D, Mori L, Puzo G, De Libero G (2005) Assistance of microbial glycolipid antigen processing by CD1e. Science 310(5752):1321-1324
39. De Jong AC, Cheng TY, Huang S, Gras S, Birkinshaw RW, Kasmar A, van Rhijn I, Peña-Cruz V, Ruan DT, Altman JD, Rossjohn J, Moody DB (2014) CD1a autoreactive T cells recognize natural skin oils that function as headless antigens. Nat Immunol 15(2):177-185
40. Haig NA, Guan Z, Li D, McMichael A, Raetz CR, Xu XN (2011) Identification of self-lipids presented by CD1c and CD1d proteins. J Biol Chem 286(43):37692-37701
41. Cox D, Fox L, Tian R, Bardet W, Skaley M, Mojsilovic D, Gumperz J, Hildebrand W (2009) Determination of cellular lipids bound to human CD1d molecules. PLoS ONe 4(5):e5325
42. Prigozy TI, Naidenko O, Qasba P, Elewaut D, Brossay L, Khurana A, Natori T, Koezuka Y, Kulkarni A, Kronenberg M (2001) Glycolipid antigen processing for presentation by CD1d molecules. Science 291(5504):664-667
43. Moody DB, Briken V, Cheng TY, Roura-Mir C, Guy MR, Geho DH, Tykocinski ML, Besra GS, Porcelli SA (2002) Lipid length controls antigen entry into endosomal and nonendosomal pathways for CD1b presentation. Nat Immunol 3(5):435-442
44. Huang S, Cheng TY, Young DC, Layre E, Madigan CA, Shires J, Cerundolo V, Altman JD, Moody DB (2011) Discovery of deoxyceramides and diacylglycerols as CD1b scaffold lipids among diverse groove-blocking lipids of the human CD1 system. Proc Natl Acad Sci USA 108(48):19335-19340
45. Zajonc DM, Cantu C 3rd, Mattner J, Zhou D, Savage PB, Bendelac A, Wilson IA, Teyton L (2005) Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat Immunol 6(8):810-818
46. Wu D, Zajonc DM, Fujio M, Sullivan BA, Kinjo Y, Kronenberg M, Wilson IA, Wong CH (2006) Design of natural killer T cell activators: structure and function of a microbial glycosphingolipid bound to mouse CD1d. Proc Natl Acad Sci USA 103(11):3972-3977
47. Garzon D, Anselmi C, Bond PJ, Faraldo-Gomez JD (2013) Dynamics of the antigen-binding grooves in CD1 proteins: reversible hydrophobic collapse in the lipid-free state. J Biol Chem 288(27):19528-19536
48. Gilleron M, Stenger S, Mazorra Z, Wittke F, Mariotti S, Bohmer G, Prandi J, Mori L, Puzo G, De Libero G (2004) Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis. J Exp Med 199(5):649-659
49. Mccarthy C, Shepherd D, Fleire S, Stronge VS, Koch M, Illarionov PA, Bossi G, Salio M, Denkberg G, Reddington F, Tarlton A, Reddy BG, Schmidt RR, Reiter Y, Griffiths GM, van der Merwe PA, Besra GS, Jones EY, Batista FD, 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(5):1131-1144
50. De Jong A, Arce EC, Cheng TY, van Summeren RP, Feringa BL, Dudkin V, Crich D, Matsunaga I, Minnaard AJ, Moody DB (2007) CD1c presentation of synthetic glycolipid antigens with foreign alkyl branching motifs. Chem Biol 14(11):1232-1242
51. Im JS, Arora P, Bricard G, Molano A, Venkataswamy MM, Baine I, Jerud ES, Goldberg MF, Baena A, Yu KO, Ndonye RM, Howell AR, Yuan W, Cresswell P, Chang YT, Illarionov PA, Besra GS, Porcelli SA (2009) Kinetics and cellular site of glycolipid loading control the outcome of natural killer T cell activation. Immunity 30(6):888-898
52. Sullivan BA, Nagarajan NA, Wingender G, Wang J, Scott I, Tsuji M, Franck RW, Porcelli SA, Zajonc DM, Kronenberg M (2010) Mechanisms for glycolipid antigen-driven cytokine polarization by valpha14i NKT cells. J Immunol 184(1):141-153
53. Relloso M, Cheng TY, Im JS, Parisini E, Roura-Mir C, DeBono C, Zajonc DM, Murga LF, Ondrechen MJ, Wilson IA, Porcelli SA, Moody DB (2008) Ph-dependent interdomain tethers of CD1b regulate its antigen capture. Immunity 28(6):774-786
54. Kang SJ, Cresswell P (2002) Calnexin, calreticulin, and eRp57 cooperate in disulfide bond formation in human CD1d heavy chain. J Biol Chem 277(47):44838-44844
55. Odyniec AN, Barral DC, Garg S, Tatituri RV, Besra GS, Brenner MB (2010) Regulation of CD1 antigen-presenting complex stability. J Biol Chem 285(16):11937-11947
56. Barral DC, Brenner MB (2007) CD1 antigen presentation: how it works. Nat Rev Immunol 7(12):929-941
57. Barral DC, Cavallari M, McCormick PJ, Garg S, Magee AI, Bonifacino JS, De Libero G, Brenner MB (2008) CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 9(9):1446-1457
58. Barral DC, Garg S, Casalou C, Watts GF, Sandoval JL, Ramalho JS, Hsu VW, Brenner MB (2012) Arl13b regulates endocytic recycling traffic. Proc Natl Acad Sci USA 109(52):21354-21359
59. Briken V, Jackman RM, Watts GF, Rogers RA, Porcelli SA (2000) Human CD1b and CD1c isoforms survey different intra-cellular compartments for the presentation of microbial lipid antigens. J Exp Med 192(2):281-288
60. Sugita M, Cao X, Watts GF, Rogers RA, Bonifacino JS, Brenner MB (2002) Failure of trafficking and antigen presentation by CD1 in AP-3-deficient cells. Immunity 16(5):697-706
61. Sugita M, van der Wel N, Rogers RA, Peters PJ, Brenner MB (2000) CD1c molecules broadly survey the endocytic system. Proc Natl Acad Sci USA 97(15):8445-8450
62. Joyce S, Woods AS, Yewdell JW, Bennink JR, De Silva AD, Boesteanu A, Balk SP, Cotter RJ, Brutkiewicz RR (1998) Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 279(5356):1541-1544
63. De Silva AD, Park JJ, Matsuki N, Stanic AK, Brutkiewicz RR, Medof ME, Joyce S (2002) Lipid protein interactions: the assembly of CD1d1 with cellular phospholipids occurs in the endoplasmic reticulum. J Immunol 168(2):723-733
64. Muindi K, Cernadas M, Watts GF, Royle L, Neville DC, Dwek RA, Besra GS, Rudd PM, Butters TD, Brenner MB (2010) Activation state and intracellular trafficking contribute to the repertoire of endogenous glycosphingolipids presented by CD1d [corrected]. Proc Natl Acad Sci USA 107(7):3052-3057
65. Yuan W, Kang SJ, Evans JE, Cresswell P (2009) Natural lipid ligands associated with human CD1d targeted to different subcellular compartments. J Immunol 182(8):4784-4791
66. Facciotti F, Ramanjaneyulu GS, Lepore M, Sansano S, Cavallari M, Kistowska M, Forss-Petter S, Ni G, Colone A, Singhal A, Berger J, Xia C, Mori L, De Libero G (2012) Peroxisome-derived lipids are self antigens that stimulate invariant natural killer T cells in the thymus. Nat Immunol 13(5):474-480
67. 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 JY, Colgan SP, Young SG, Exley M, Blumberg RS (2004) CD1d function is regulated by microsomal triglyceride transfer protein. Nat Med 10(5):535-539
68. Hussain MM, Rava P, Pan X, Dai K, Dougan SK, Iqbal J, Lazare F, Khatun I (2008) Microsomal triglyceride transfer protein in plasma and cellular lipid metabolism. Curr Opin Lipidol 19(3):277-284
69. Dougan SK, Salas A, Rava P, Agyemang A, Kaser A, Morrison J, Khurana A, Kronenberg M, Johnson C, Exley M, Hussain MM, Blumberg RS (2005) Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells. J Exp Med 202(4):529-539
70. Zeissig S, Dougan SK, Barral DC, Junker Y, Chen Z, Kaser A, Ho M, Mandel H, McIntyre A, Kennedy SM, Painter GF, Veerapen N, Besra GS, Cerundolo V, Yue S, Beladi S, Behar SM, Chen X, Gumperz JE, Breckpot K, Raper A, Baer A, Exley MA, Hegele RA, Cuchel M, Rader DJ, Davidson NO, Blumberg RS (2010) Primary deficiency of microsomal triglyceride transfer protein in human abetalipoproteinemia is associated with loss of CD1 function. J Clin Invest 120(8):2889-2899
71. Sagiv Y, Bai L, Wei DG, Agami R, Savage PB, Teyton L, Bendelac A (2007) A distal effect of microsomal triglyceride transfer protein deficiency on the lysosomal recycling of CD1d. J Exp Med 204(4):921-928
72. Kaser A, Hava DL, Dougan SK, Chen Z, Zeissig S, Brenner MB, Blumberg RS (2008) Microsomal triglyceride transfer protein regulates endogenous and exogenous antigen presentation by group 1 CD1 molecules. Eur J Immunol 38(8):2351-2359
73. Cernadas M, Cavallari M, Watts G, Mori L, De Libero G, Brenner MB (2010) Early recycling compartment trafficking of CD1a is essential for its intersection and presentation of lipid antigens. J Immunol 184(3):1235-1241
74. Ernst WA, Maher J, Cho S, Niazi KR, Chatterjee D, Moody DB, Besra GS, Watanabe Y, Jensen PE, Porcelli SA, Kronenberg M, Modlin RL (1998) Molecular interaction of CD1b with lipoglycan antigens. Immunity 8(3):331-340
75. Kang SJ, Cresswell P (2004) Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat Immunol 5(2):175-181
76. Winau F, Schwierzeck V, Hurwitz R, Remmel N, Sieling PA, Modlin RL, Porcelli SA, Brinkmann V, Sugita M, Sandhoff K, Kaufmann SH, Schaible UE (2004) Saposin C is required for lipid presentation by human CD1b. Nat Immunol 5(2):169-174
77. Zhou D, Cantu C 3rd, Sagiv Y, Schrantz N, Kulkarni AB, Qi X, Mahuran DJ, Morales CR, Grabowski GA, Benlagha K, Savage P, Bendelac A, Teyton L (2004) Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 303(5657):523-527
78. Leon L, Tatituri RV, Grenha R, Sun Y, Barral DC, Minnaard AJ, Bhowruth V, Veerapen N, Besra GS, Kasmar A, Peng W, Moody DB, Grabowski GA, Brenner MB (2012) Saposins utilize two strategies for lipid transfer and CD1 antigen presentation. Proc Natl Acad Sci USA 109(12):4357-4364
79. Darmoise A, Teneberg S, Bouzonville L, Brady RO, Beck M, Kaufmann SH, Winau F (2010) Lysosomal alpha-galactosidase controls the generation of self lipid antigens for natural killer T cells. Immunity 33(2):216-228
80. Zhou D, Mattner J, Cantu C 3rd, Schrantz N, Yin N, Gao Y, Sagiv Y, Hudspeth K, Wu YP, Yamashita T, Teneberg S, Wang D, Proia RL, Levery SB, Savage PB, Teyton L, Bendelac A (2004) Lysosomal glycosphingolipid recognition by NKT cells. Science 306(5702):1786-1789
81. De Jong A, Pena-Cruz V, Cheng TY, Clark RA, van Rhijn I, Moody DB (2010) CD1a-autoreactive T cells are a normal component of the human alphabeta T cell repertoire. Nat Immunol 11(12):1102-1109
82. De Lalla C, Lepore M, Piccolo FM, Rinaldi A, Scelfo A, Garavaglia C, Mori L, De Libero G, Dellabona P, Casorati G (2011) High-frequency and adaptive-like dynamics of human CD1 self-reactive T cells. Eur J Immunol 41(3):602-610
83. Lockridge JL, Chen X, Zhou Y, Rajesh D, Roenneburg DA et al (2011) Analysis of the CD1 Antigen Presenting System in Humanized SCID Mice. PLoS ONe 6(6):e21701
84. Felio K, Nguyen H, Dascher CC, Choi HJ, Li S, Zimmer MI, Colmone A, Moody DB, Brenner MB, Wang CR (2009) CD1-restricted adaptive immune responses to mycobacteria in human group 1 CD1 transgenic mice. J Exp Med 206(11):2497-2509
85. Kasmar AG, van Rhijn I, Cheng TY, Turner M, Seshadri C, Schiefner A, Kalathur RC, Annand JW, de Jong A, Shires J, Leon L, Brenner M, Wilson IA, Altman JD, Moody DB (2011) CD1b tetramers bind alphabeta T cell receptors to identify a mycobacterial glycolipid-reactive T cell repertoire in humans. J Exp Med 208(9):1741-1747
86. Gumperz JE, Miyake S, Yamamura T, Brenner MB (2002) Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining. J Exp Med 195(5):625-636
87. Kasmar AG, van Rhijn I, Magalhaes KG, Young DC, Cheng TY, Turner MT, Schiefner A, Kalathur RC, Wilson IA, Bhati M, Gras S, Birkinshaw RW, Tan LL, Rossjohn J, Shires J, Jakobsen S, Altman JD, Moody DB (2013) Cutting edge: CD1a tetramers and dextramers identify human lipopeptide-specific T cells ex vivo. J Immunol 191(9):4499-4503