Immunogenetics

, Volume 68, Issue 8, pp 561–576 | Cite as

The CD1 family: serving lipid antigens to T cells since the Mesozoic era

Review

Abstract

Class I-like CD1 molecules are in a family of antigen-presenting molecules that bind lipids and lipopeptides, rather than peptides for immune surveillance by T cells. Since CD1 lacks the high degree of polymorphism found in their major histocompatibility complex (MHC) class I molecules, different species express different numbers of CD1 isotypes, likely to be able to present structurally diverse classes of lipid antigens. In this review, we will present a historical overview of the structures of the different human CD1 isotypes and also discuss species-specific adaptations of the lipid-binding groove. We will discuss how single amino acid changes alter the shape and volume of the CD1 binding groove, how these minor changes can give rise to different numbers of binding pockets, and how these pockets affect the lipid repertoire that can be presented by any given CD1 protein. We will compare the structures of various lipid antigens and finally, we will discuss recognition of CD1-presented lipid antigens by antigen receptors on T cells (TCRs).

Keywords

CD1 isoforms TCR recognition Lipid antigens Lipid-binding pockets 

References

  1. Adams EJ, Gu S, Luoma AM (2015) Human gamma delta T cells: evolution and ligand recognition. Cell Immunol. doi:10.1016/j.cellimm.2015.04.008 PubMedCentralGoogle Scholar
  2. Adams EJ, Luoma AM (2013) The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules. Annu Rev Immunol 31:529–561. doi:10.1146/annurev-immunol-032712-095912 PubMedCrossRefGoogle Scholar
  3. Agea E et al. (2005) Human CD1-restricted T cell recognition of lipids from pollens. J Exp Med 202:295–308PubMedPubMedCentralCrossRefGoogle Scholar
  4. Angenieux C et al. (2005) The cellular pathway of CD1e in immature and maturing dendritic cells. Traffic 6:286–302PubMedCrossRefGoogle Scholar
  5. Angenieux C, Salamero J, Fricker D, Cazenave JP, Goud B, Hanau D, de La Salle H (2000) Characterization of CD1e, a third type of CD1 molecule expressed in dendritic cells. J Biol Chem 275:37757–37764PubMedCrossRefGoogle Scholar
  6. Arrenberg P, Halder R, Dai Y, Maricic I, Kumar V (2010) Oligoclonality and innate-like features in the TCR repertoire of type II NKT cells reactive to a beta-linked self-glycolipid. Proc Natl Acad Sci U S A 107:10984–10989. doi:10.1073/pnas.1000576107 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Arrenberg P, Maricic I, Kumar V (2011) Sulfatide-mediated activation of type II natural killer T cells prevents hepatic ischemic reperfusion injury in mice. Gastroenterology 140:646–655. doi:10.1053/j.gastro.2010.10.003 PubMedCrossRefGoogle Scholar
  8. Aspeslagh S et al. (2011) Galactose-modified iNKT cell agonists stabilized by an induced fit of CD1d prevent tumour metastasis. EMBO J 30:2294–2305. doi:10.1038/emboj.2011.145 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Aspeslagh S et al. (2013) Enhanced TCR footprint by a novel glycolipid increases NKT-dependent tumor protection. J Immunol 191:2916–2925. doi:10.4049/jimmunol.1203134 PubMedCrossRefGoogle Scholar
  10. Barral DC et al. (2008) CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 9:1446–1457. doi:10.1111/j.1600-0854.2008.00781.x PubMedCrossRefGoogle Scholar
  11. Batuwangala T et al. (2004) The crystal structure of human CD1b with a bound bacterial glycolipid. J Immunol 172:2382–2388PubMedCrossRefGoogle Scholar
  12. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25:297–336PubMedCrossRefGoogle Scholar
  13. Birkinshaw RW et al. (2015) Alphabeta T cell antigen receptor recognition of CD1a presenting self lipid ligands. Nat Immunol 16:258–266. doi:10.1038/ni.3098 PubMedCrossRefGoogle Scholar
  14. Blomqvist M et al. (2009) Multiple tissue-specific isoforms of sulfatide activate CD1d-restricted type II NKT cells. Eur J Immunol 39:1726–1735. doi:10.1002/eji.200839001 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Borg NA et al. (2007) CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature 448:44–49PubMedCrossRefGoogle Scholar
  16. Bourgeois EA et al. (2015) Bee venom processes human skin lipids for presentation by CD1a. J Exp Med 212:149–163. doi:10.1084/jem.20141505 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bradbury A, Belt KT, Neri TM, Milstein C, Calabi F (1988) Mouse CD1 is distinct from and co-exists with TL in the same thymus. EMBO J 7:3081–3086PubMedPubMedCentralGoogle Scholar
  18. Brigl M, Brenner MB (2004) CD1: antigen presentation and T cell function. Annu Rev Immunol 22:817–890PubMedCrossRefGoogle Scholar
  19. Brozovic S et al. (2004) CD1d function is regulated by microsomal triglyceride transfer protein. Nat Med 10:535–539PubMedCrossRefGoogle Scholar
  20. Calabi F, Jarvis JM, Martin L, Milstein C (1989) Two classes of CD1 genes. Eur J Immunol 19:285–292PubMedCrossRefGoogle Scholar
  21. Calabi F, Milstein C (1986) A novel family of human major histocompatibility complex-related genes not mapping to chromosome 6. Nature 323:540–543. doi:10.1038/323540a0 PubMedCrossRefGoogle Scholar
  22. Cardell S, Tangri S, Chan S, Kronenberg M, Benoist C, Mathis D (1995) CD1-restricted CD4+ T cells in major histocompatibility complex class II-deficient mice. J Exp Med 182:993–1004PubMedCrossRefGoogle Scholar
  23. Chang YJ et al. (2011) Influenza infection in suckling mice expands an NKT cell subset that protects against airway hyperreactivity. J Clin Invest 121:57–69. doi:10.1172/JCI44845 PubMedCrossRefGoogle Scholar
  24. Dascher CC (2007) Evolutionary biology of CD1. Curr Top Microbiol Immunol 314:3–26PubMedGoogle Scholar
  25. Dascher CC et al. (1999) Conservation of a CD1 multigene family in the guinea pig. J Immunol 163:5478–5488PubMedGoogle Scholar
  26. de Jong A et al. (2014) CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens. Nat Immunol 15:177–185. doi:10.1038/ni.2790 PubMedCrossRefGoogle Scholar
  27. de la Salle H et al. (2005) Assistance of microbial glycolipid antigen processing by CD1e. Science 310:1321–1324PubMedCrossRefGoogle Scholar
  28. de Lalla C et al. (2011) High-frequency and adaptive-like dynamics of human CD1 self-reactive T cells. Eur J Immunol 41:602–610. doi:10.1002/eji.201041211 PubMedCrossRefGoogle Scholar
  29. Dieude M et al. (2011) Cardiolipin binds to CD1d and stimulates CD1d-restricted gammadelta T cells in the normal murine repertoire. J Immunol 186:4771–4781. doi:10.4049/jimmunol.1000921 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dougan SK et al. (2005) Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells. J Exp Med 202:529–539PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dvir H, Wang J, Ly N, Dascher CC, Zajonc DM (2010) Structural basis for lipid-antigen recognition in avian immunity. J Immunol 184:2504–2511. doi:10.4049/jimmunol.0903509 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Ernst WA et al. (1998) Molecular interaction of CD1b with lipoglycan antigens. Immunity 8:331–340PubMedCrossRefGoogle Scholar
  33. Facciotti F et al. (2011) Fine tuning by human CD1e of lipid-specific immune responses. Proc Natl Acad Sci U S A 108:14228–14233. doi:10.1073/pnas.1108809108 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fischer K et al. (2004) Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc Natl Acad Sci U S A 101:10685–10690PubMedPubMedCentralCrossRefGoogle Scholar
  35. Freigang S et al. (2010) Fatty acid amide hydrolase shapes NKT cell responses by influencing the serum transport of lipid antigen in mice. J Clin Invest 120:1873–1884. doi:10.1172/JCI40451 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gadola SD et al. (2002) Structure of human CD1b with bound ligands at 2.3 Å, a maze for alkyl chains. Nat Immunol 3:721–726PubMedCrossRefGoogle Scholar
  37. Garcia-Alles LF et al. (2011a) Structural reorganization of the antigen-binding groove of human CD1b for presentation of mycobacterial sulfoglycolipids. Proc Natl Acad Sci U S A 108:17755–17760. doi:10.1073/pnas.1110118108 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Garcia-Alles LF et al. (2011b) Crystal structure of human CD1e reveals a groove suited for lipid-exchange processes. Proc Natl Acad Sci U S A 108:13230–13235. doi:10.1073/pnas.1105627108 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Garcia-Alles LF et al. (2006) Endogenous phosphatidylcholine and a long spacer ligand stabilize the lipid-binding groove of CD1b. EMBO J 25:3684–3692PubMedPubMedCentralCrossRefGoogle Scholar
  40. Giabbai B et al. (2005) Crystal structure of mouse CD1d bound to the self ligand phosphatidylcholine: a molecular basis for NKT cell activation. J Immunol 175:977–984PubMedCrossRefGoogle Scholar
  41. Gilleron M et al. (2004) Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis. J Exp Med 199:649–659PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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 13:851–856. doi:10.1038/ni.2371 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Girardi E et al. (2010) Crystal structure of bovine CD1b3 with endogenously bound ligands. J Immunol 185:376–386. doi:10.4049/jimmunol.1000042 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Girardi E, Wang J, Zajonc DM (2016) Structure of an alpha-helical peptide and lipopeptide bound to the non-classical MHC class I molecule CD1d. J Biol Chem. doi:10.1074/jbc.M115.702118 PubMedGoogle Scholar
  45. Girardi E et al. (2011) Unique interplay between sugar and lipid in determining the antigenic potency of bacterial antigens for NKT cells. PLoS Biol 9:e1001189. doi:10.1371/journal.pbio.1001189 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Girardi E, Zajonc DM (2012) Molecular basis of lipid antigen presentation by CD1d and recognition by natural killer T cells. Immunol Rev 250:167–179. doi:10.1111/j.1600-065X.2012.01166.x PubMedPubMedCentralCrossRefGoogle Scholar
  47. Goff RD et al. (2004) Effects of lipid chain lengths in α-galactosylceramides on cytokine release by natural killer T cells. J Am Chem Soc 126:13602–13603PubMedCrossRefGoogle Scholar
  48. Gumperz JE et al. (2000) Murine CD1d-restricted T cell recognition of cellular lipids. Immunity 12:211–221PubMedCrossRefGoogle Scholar
  49. Hee CS, Gao S, Loll B, Miller MM, Uchanska-Ziegler B, Daumke O, Ziegler A (2010) Structure of a classical MHC class I molecule that binds “non-classical” ligands. PLoS Biol 8:e1000557. doi:10.1371/journal.pbio.1000557 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Ito Y et al. (2013) Helicobacter pylori cholesteryl alpha-glucosides contribute to its pathogenicity and immune response by natural killer T cells. PLoS One 8:e78191. doi:10.1371/journal.pone.0078191 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Jackman RM et al. (1998) The tyrosine-containing cytoplasmic tail of CD1b is essential for its efficient presentation of bacterial lipid antigens. Immunity 8:341–351PubMedCrossRefGoogle Scholar
  52. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, Kumar V (2004) Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide. J Exp Med 199:947–957PubMedPubMedCentralCrossRefGoogle Scholar
  53. Jahng AW et al. (2001) Activation of natural killer T cells potentiates or prevents experimental autoimmune encephalomyelitis. J Exp Med 194:1789–1799PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jarrett R et al. (2016) Filaggrin inhibits generation of CD1a neolipid antigens by house dust mite-derived phospholipase. Sci Transl Med 8:–325ra318Google Scholar
  55. Joyce S et al. (1998) Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 279:1541–1544PubMedCrossRefGoogle Scholar
  56. Kain L et al. (2014) The identification of the endogenous ligands of natural killer T cells reveals the presence of mammalian alpha-linked glycosylceramides. Immunity 41:543–554. doi:10.1016/j.immuni.2014.08.017 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kang SJ, Cresswell P (2004) Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat Immunol 5:175–181PubMedCrossRefGoogle Scholar
  58. Kasmar AG et al. (2011) CD1b tetramers bind alphabeta T cell receptors to identify a mycobacterial glycolipid-reactive T cell repertoire in humans. J Exp Med 208:1741–1747. doi:10.1084/jem.20110665 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kawano T et al. (1997) CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 278:1626–1629PubMedCrossRefGoogle Scholar
  60. Kerzerho J et al. (2012) Structural and functional characterization of a novel nonglycosidic type I NKT agonist with immunomodulatory properties. J Immunol 188:2254–2265. doi:10.4049/jimmunol.1103049 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kinjo Y et al. (2011) Invariant natural killer T cells recognize glycolipids from pathogenic gram-positive bacteria. Nat Immunol 12:966–974. doi:10.1038/ni.2096 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kinjo Y et al. (2006) Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat Immunol 7:978–986PubMedCrossRefGoogle Scholar
  63. Kinjo Y et al. (2005) Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 434:520–525. doi:10.1038/nature03407 PubMedCrossRefGoogle Scholar
  64. Koch M et al. (2005) The crystal structure of human CD1d with and without α-galactosylceramide. Nat Immunol 8:819–826CrossRefGoogle Scholar
  65. Li Y, Girardi E, Wang J, Yu ED, Painter GF, Kronenberg M, Zajonc DM (2010) The Vα14 invariant natural killer T cell TCR forces microbial glycolipids and CD1d into a conserved binding mode. J Exp Med 207:2383–2393. doi:10.1084/jem.20101335 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 31:2047–2059. doi:10.1038/emboj.2012.54 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Luoma AM et al. (2013) Crystal structure of Vdelta1 T cell receptor in complex with CD1d-sulfatide shows MHC-like recognition of a self-lipid by human gammadelta T cells. Immunity 39:1032–1042. doi:10.1016/j.immuni.2013.11.001 PubMedCrossRefGoogle Scholar
  68. Ly D et al. (2013) CD1c tetramers detect ex vivo T cell responses to processed phosphomycoketide antigens. J Exp Med 210:729–741. doi:10.1084/jem.20120624 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mallevaey T et al. (2011) A molecular basis for NKT cell recognition of CD1d-self-antigen. Immunity 34:315–326. doi:10.1016/j.immuni.2011.01.013 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Mansour S et al. (2016) Cholesteryl esters stabilize human CD1c conformations for recognition by self-reactive T cells. Proc Natl Acad Sci U S A 113:E1266–E1275. doi:10.1073/pnas.1519246113 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Maricic I, Girardi E, Zajonc DM, Kumar V (2014) Recognition of lysophosphatidylcholine by type II NKT cells and protection from an inflammatory liver disease. J Immunol 193:4580–4589. doi:10.4049/jimmunol.1400699 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Maruoka T, Tanabe H, Chiba M, Kasahara M (2005) Chicken CD1 genes are located in the MHC: CD1 and endothelial protein C receptor genes constitute a distinct subfamily of class-I-like genes that predates the emergence of mammals. Immunogenetics 57:590–600PubMedCrossRefGoogle Scholar
  73. Matsuda JL et al. (2000) Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J Exp Med 192:741–754PubMedPubMedCentralCrossRefGoogle Scholar
  74. Matsunaga I et al. (2004) Mycobacterium tuberculosis pks12 produces a novel polyketide presented by CD1c to T cells. J Exp Med 200:1559–1569PubMedPubMedCentralCrossRefGoogle Scholar
  75. Mattner J et al. (2005) Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434:525–529PubMedCrossRefGoogle Scholar
  76. Maxfield FR, Hao M (2013) Lipid trafficking in cells. In: Roberts GCK (ed) Encyclopedia of biophysics. Springer, Berlin Heidelberg, pp. 1289–1296. doi:10.1007/978-3-642-16712-6_651 CrossRefGoogle Scholar
  77. Miller MM et al. (2005) Characterization of two avian MHC-like genes reveals an ancient origin of the CD1 family. Proc Natl Acad Sci U S A 102:8674–8679PubMedPubMedCentralCrossRefGoogle Scholar
  78. Miyamoto K, Miyake S, Yamamura T (2001) A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 413:531–534PubMedCrossRefGoogle Scholar
  79. Moody DB (2001) Polyisoprenyl glycolipids as targets of CD1-mediated T cell responses. Cell Mol Life Sci 58:1461–1474PubMedCrossRefGoogle Scholar
  80. Moody DB, Porcelli SA (2003) Intracellular pathways of CD1 antigen presentation. Nat Rev Immunol 3:11–22PubMedCrossRefGoogle Scholar
  81. Moody DB et al. (1997) Structural requirements for glycolipid antigen recognition by CD1b- restricted T cells. Science 278:283–286PubMedCrossRefGoogle Scholar
  82. Moody DB et al. (2000) CD1c-mediated T-cell recognition of isoprenoid glycolipids in Mycobacterium tuberculosis infection. Nature 404:884–888PubMedCrossRefGoogle Scholar
  83. Moody DB et al. (2004) T cell activation by lipopeptide antigens. Science 303:527–531PubMedCrossRefGoogle Scholar
  84. Moody DB, Zajonc DM, Wilson IA (2005) Anatomy of CD1-lipid antigen complexes. Nat Rev Immunol 5:387–399PubMedCrossRefGoogle Scholar
  85. Mori L, Lepore M, De Libero G (2016) The immunology of CD1- and MR1-restricted T cells. Annu Rev Immunol 34:479–510. doi:10.1146/annurev-immunol-032414-112008 PubMedCrossRefGoogle Scholar
  86. Nguyen TK et al. (2012) The bovine CD1D gene has an unusual gene structure and is expressed but cannot present alpha-galactosylceramide with a C26 fatty acid. Int Immunol. doi:10.1093/intimm/dxs092 PubMedPubMedCentralGoogle Scholar
  87. Patel O et al. (2011) NKT TCR recognition of CD1d-alpha-C-galactosylceramide. J Immunol 187:4705–4713. doi:10.4049/jimmunol.1100794 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Patel O et al. (2012) Recognition of CD1d-sulfatide mediated by a type II natural killer T cell antigen receptor. Nat Immunol 13:857–863. doi:10.1038/ni.2372 PubMedCrossRefGoogle Scholar
  89. Pellicci DG et al. (2011) Recognition of beta-linked self glycolipids mediated by natural killer T cell antigen receptors. Nat Immunol 12:827–833. doi:10.1038/ni.2076 PubMedCrossRefGoogle Scholar
  90. Pellicci DG et al. (2009) Differential recognition of CD1d-alpha-galactosyl ceramide by the V beta 8.2 and V beta 7 semi-invariant NKT T cell receptors. Immunity 31:47–59. doi:10.1016/j.immuni.2009.04.018 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pellicci DG et al. (2014) The molecular bases of delta/alphabeta T cell-mediated antigen recognition. J Exp Med 211:2599–2615. doi:10.1084/jem.20141764 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Rauch J et al. (2003) Structural features of the acyl chain determine self-phospholipid antigen recognition by a CD1d-restricted invariant NKT (iNKT) cell. J Biol Chem 278:47508–47515PubMedPubMedCentralCrossRefGoogle Scholar
  93. Reinink P, Van Rhijn I (2009) The bovine T cell receptor alpha/delta locus contains over 400 V genes and encodes V genes without CDR2. Immunogenetics 61:541–549. doi:10.1007/s00251-009-0384-9 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Reinink P, Van Rhijn I (2016) Mammalian CD1 and MR1 genes. doi:10.1007/s00251-016-0926-x
  95. Rhost S et al. (2012) Identification of novel glycolipid ligands activating a sulfatide-reactive, CD1d-restricted, type II natural killer T lymphocyte. Eur J Immunol 42:2851–2860. doi:10.1002/eji.201142350 PubMedCrossRefGoogle Scholar
  96. Rossjohn J, Gras S, Miles JJ, Turner SJ, Godfrey DI, McCluskey J (2015) T cell antigen receptor recognition of antigen-presenting molecules. Annu Rev Immunol 33:169–200. doi:10.1146/annurev-immunol-032414-112334 PubMedCrossRefGoogle Scholar
  97. Roy S, Ly D, Li NS, Altman JD, Piccirilli JA, Moody DB, Adams EJ (2014) Molecular basis of mycobacterial lipid antigen presentation by CD1c and its recognition by alphabeta T cells. Proc Natl Acad Sci U S A 111:E4648–E4657. doi:10.1073/pnas.1408549111 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Salamero J et al. (2001) CD1a molecules traffic through the early recycling endosomal pathway in human Langerhans cells. J Investig Dermatol 116:401–408PubMedCrossRefGoogle Scholar
  99. Salomonsen J et al. (2005) Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC. Proc Natl Acad Sci U S A 102:8668–8673PubMedPubMedCentralCrossRefGoogle Scholar
  100. Scharf L et al. (2010) The 2.5 a structure of CD1c in complex with a mycobacterial lipid reveals an open groove ideally suited for diverse antigen presentation. Immunity 33:853–862. doi:10.1016/j.immuni.2010.11.026 PubMedPubMedCentralCrossRefGoogle Scholar
  101. Schiefner A, Fujio M, Wu D, Wong CH, Wilson IA (2009) Structural evaluation of potent NKT cell agonists: implications for design of novel stimulatory ligands. J Mol Biol 394:71–82. doi:10.1016/j.jmb.2009.08.061 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Schmieg J, Yang G, Franck RW, Tsuji M (2003) Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand α-galactosylceramide. J Exp Med 198:1631–1641PubMedPubMedCentralCrossRefGoogle Scholar
  103. Scott-Browne JP et al. (2007) Germline-encoded recognition of diverse glycolipids by natural killer T cells. Nat Immunol 8:1105–1113PubMedCrossRefGoogle Scholar
  104. Shamshiev A, Donda A, Carena I, Mori L, Kappos L, De Libero G (1999) Self glycolipids as T-cell autoantigens. Eur J Immunol 29:1667–1675PubMedCrossRefGoogle Scholar
  105. Shamshiev A, Gober HJ, Donda A, Mazorra Z, Mori L, De Libero G (2002) Presentation of the same glycolipid by different CD1 molecules. J Exp Med 195:1013–1021PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sieling PA et al. (1995) CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 269:227–230PubMedCrossRefGoogle Scholar
  107. Sriram V, Du W, Gervay-Hague J, Brutkiewicz RR (2005) Cell wall glycosphingolipids of Sphingomonas paucimobilis are CD1d-specific ligands for NKT cells. Eur J Immunol 35:1692–1701PubMedCrossRefGoogle Scholar
  108. Sugita M, Cernadas M, Brenner MB (2004) New insights into pathways for CD1-mediated antigen presentation. Curr Opin Immunol 16:90–95PubMedCrossRefGoogle Scholar
  109. Sugita M, Grant EP, van Donselaar E, Hsu VW, Rogers RA, Peters PJ, Brenner MB (1999) Separate pathways for antigen presentation by CD1 molecules. Immunity 11:743–752PubMedCrossRefGoogle Scholar
  110. Sullivan BA et al. (2010) Mechanisms for glycolipid antigen-driven cytokine polarization by Vα14i NKT cells. J Immunol 184:141–153. doi:10.4049/jimmunol.0902880 PubMedCrossRefGoogle Scholar
  111. Uldrich AP et al. (2013) CD1d-lipid antigen recognition by the γδ TCR. Nat Immunol. doi:10.1038/ni.2713 PubMedGoogle Scholar
  112. van den Elzen P et al. (2005) Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 437:906–910PubMedCrossRefGoogle Scholar
  113. Van Rhijn I et al. (2013) A conserved human T cell population targets mycobacterial antigens presented by CD1b. Nat Immunol 14:706–713. doi:10.1038/ni.2630 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Van Rhijn I et al. (2006) The bovine CD1 family contains group 1 CD1 proteins, but no functional CD1d. J Immunol 176:4888–4893PubMedCrossRefGoogle Scholar
  115. Van Rhijn I, Zajonc DM, Wilson IA, Moody DB (2005) T-cell activation by lipopeptide antigens. Curr Opin Immunol 17:222–229PubMedCrossRefGoogle Scholar
  116. Wang J, Guillaume J, Pauwels N, Van Calenbergh S, Van Rhijn I, Zajonc DM (2012) Crystal structures of bovine CD1d reveal altered alphaGalCer presentation and a restricted A′ pocket unable to bind long-chain glycolipids. PLoS One 7:e47989. doi:10.1371/journal.pone.0047989 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Wang J et al. (2010) Lipid binding orientation within CD1d affects recognition of Borrelia burgdorferi antigens by NKT cells. Proc Natl Acad Sci U S A 107:1535–1540. doi:10.1073/pnas.0909479107 PubMedCrossRefGoogle Scholar
  118. Winau F et al. (2004) Saposin C is required for lipid presentation by human CD1b. Nat Immunol 5:169–174PubMedCrossRefGoogle Scholar
  119. Wu D et al. (2005) Bacterial glycolipids and analogs as antigens for CD1d-restricted NKT cells. Proc Natl Acad Sci U S A 102:1351–1356PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wu D et al. (2006) Design of natural killer T cell activators: structure and function of a microbial glycosphingolipid bound to mouse CD1d. Proc Natl Acad Sci U S A 103:3972–3977. doi:10.1073/pnas.0600285103 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Wu DY, Segal NH, Sidobre S, Kronenberg M, Chapman PB (2003) Cross-presentation of disialoganglioside GD3 to natural killer T cells. J Exp Med 198:173–181PubMedPubMedCentralCrossRefGoogle Scholar
  122. Wun KS et al. (2008) A minimal binding footprint on CD1d-glycolipid is a basis for selection of the unique human NKT TCR. J Exp Med 205:939–949. doi:10.1084/jem.20072141 PubMedPubMedCentralCrossRefGoogle Scholar
  123. Wun KS et al. (2011) A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells. Immunity 34:327–339. doi:10.1016/j.immuni.2011.02.001 PubMedPubMedCentralCrossRefGoogle Scholar
  124. Wun KS et al. (2012) Human and mouse type I natural killer T cell antigen receptors exhibit different fine specificities for CD1d-antigen complex. J Biol Chem 287:39139–39148. doi:10.1074/jbc.M112.412320 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Yang Z et al. (2015) Analysis of the reptile CD1 genes: evolutionary implications. Immunogenetics 67:337–346. doi:10.1007/s00251-015-0837-2 PubMedCrossRefGoogle Scholar
  126. Young MH, Gapin L (2011) Group 1 CD1-restricted T cells take center stage. Eur J Immunol. doi:10.1002/eji.201041408 PubMedGoogle Scholar
  127. Yu ED, Girardi E, Wang J, Zajonc DM (2011) Cutting edge: structural basis for the recognition of {beta}-linked glycolipid antigens by invariant NKT cells. J Immunol 187:2079–2083. doi:10.4049/jimmunol.1101636 PubMedPubMedCentralCrossRefGoogle Scholar
  128. Yu KO et al. (2005) Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of α-galactosylceramides. Proc Natl Acad Sci U S A 102:3383–3388PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zajonc DM, Ainge GD, Painter GF, Severn WB, Wilson IA (2006) Structural characterization of mycobacterial phosphatidylinositol mannoside binding to mouse CD1d. J Immunol 177:4577–4583PubMedCrossRefGoogle Scholar
  130. Zajonc DM et al. (2005a) Structure and function of a potent agonist for the semi-invariant natural killer T cell receptor. Nat Immunol 8:810–818CrossRefGoogle Scholar
  131. Zajonc DM et al. (2005b) Molecular mechanism of lipopeptide presentation by CD1a. Immunity 22:209–219PubMedCrossRefGoogle Scholar
  132. 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 Å. Nat Immunol 4:808–815PubMedCrossRefGoogle Scholar
  133. Zajonc DM, Girardi E (2015) Recognition of microbial glycolipids by natural killer T cells. Front Immunol 6:400. doi:10.3389/fimmu.2015.00400 PubMedPubMedCentralCrossRefGoogle Scholar
  134. Zajonc DM et al. (2005c) Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity. J Exp Med 202:1517–1526. doi:10.1084/jem.20051625 PubMedPubMedCentralCrossRefGoogle Scholar
  135. Zajonc DM, Savage PB, Bendelac A, Wilson IA, Teyton L (2008a) Crystal structures of mouse CD1d-iGb3 complex and its cognate Vα14 T cell receptor suggest a model for dual recognition of foreign and self glycolipids. J Mol Biol 377:1104–1116. doi:10.1016/j.jmb.2008.01.061 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Zajonc DM, Striegl H, Dascher CC, Wilson IA (2008b) The crystal structure of avian CD1 reveals a smaller, more primordial antigen-binding pocket compared to mammalian CD1. Proc Natl Acad Sci U S A 105:17925–17930. doi:10.1073/pnas.0809814105 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Zajonc DM, Wilson IA (2007) Architecture of CD1 proteins. Curr Top Microbiol Immunol 314:27–50PubMedGoogle Scholar
  138. 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 277:339–345PubMedCrossRefGoogle Scholar
  139. Zhou D et al. (2004a) Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 303:523–527PubMedCrossRefGoogle Scholar
  140. Zhou D et al. (2004b) Lysosomal glycosphingolipid recognition by NKT cells. Science 306:1786–1789PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Division of Cell BiologyLa Jolla Institute for Allergy and Immunology (LJI)La JollaUSA
  2. 2.Department of Internal Medicine, Faculty of Medicine and Health SciencesGhent UniversityGhentBelgium

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