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Journal of Immunology Research
Volume 2016 (2016), Article ID 2876275, 11 pages
http://dx.doi.org/10.1155/2016/2876275
Review Article

CD1-Restricted T Cells at the Crossroad of Innate and Adaptive Immunity

Catia S. Pereira1,2 and M. Fatima Macedo1,2,3

1Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
2Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Porto, Portugal
3Departamento de Ciências Médicas, Universidade de Aveiro, Aveiro, Portugal

Received 8 August 2016; Accepted 13 November 2016

Academic Editor: Mikhail M. Dikov

Copyright © 2016 Catia S. Pereira and M. Fatima Macedo. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Porcelli, M. B. Brenner, J. L. Greenstein, S. P. Balk, C. Terhorst, and P. A. Bleicher, “Recognition of cluster of differentiation 1 antigens by human CD4−CD8− cytolytic T lymphocyte,” Nature, vol. 341, no. 6241, pp. 447–450, 1989. View at Publisher · View at Google Scholar · View at Scopus
  2. E. M. Beckman, S. A. Porcelli, C. T. Morita, S. M. Behar, S. T. Furlong, and M. B. Brenner, “Recognition of a lipid antigen by CD1-restricted αβ+ T cells,” Nature, vol. 372, no. 6507, pp. 691–694, 1994. View at Publisher · View at Google Scholar · View at Scopus
  3. G. De Libero and L. Mori, “The T-cell response to lipid antigens of Mycobacterium tuberculosis,” Frontiers in Immunology, vol. 5, article 219, p. 1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Mori, M. Lepore, and G. De Libero, “The immunology of CD1- and MR1-restricted T cells,” Annual Review of Immunology, vol. 34, no. 1, pp. 479–510, 2016. View at Publisher · View at Google Scholar
  5. S. K. Dougan, A. Kaser, and R. S. Blumberg, “CD1 expression on antigen-presenting cells,” Current Topics in Microbiology and Immunology, vol. 314, pp. 113–141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Rakhshandehroo, S. M. W. Gijzel, R. Siersbæk et al., “CD1d-mediated presentation of endogenous lipid antigens by adipocytes requires microsomal triglyceride transfer protein,” The Journal of Biological Chemistry, vol. 289, no. 32, pp. 22128–22139, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Y. Huh, J. I. Kim, Y. J. Park et al., “A novel function of adipocytes in lipid antigen presentation to iNKT cells,” Molecular and Cellular Biology, vol. 33, no. 2, pp. 328–339, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. H. De La Salle, S. Mariotti, C. Angenieux et al., “Assistance of microbial glycolipid antigen processing by CD1e,” Science, vol. 310, no. 5752, pp. 1321–1324, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Ly and D. B. Moody, “The CD1 size problem: lipid antigens, ligands, and scaffolds,” Cellular and Molecular Life Sciences, vol. 71, no. 16, pp. 3069–3079, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Mori and G. De Libero, “T cells specific for lipid antigens,” Immunologic Research, vol. 53, no. 1-3, pp. 191–199, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Batuwangala, D. Shepherd, S. D. Gadola et al., “The crystal structure of human CD1b with a bound bacterial glycolipid,” The Journal of Immunology, vol. 172, no. 4, pp. 2382–2388, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. D. M. Zajonc, M. A. Elsliger, L. Teyton, and I. A. Wilson, “Crystal structure of CD1a in complex with a sulfatide self antigen at a resolution of 2.15 Å,” Nature Immunology, vol. 4, no. 8, pp. 808–815, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Salio, J. D. Silk, E. Yvonne Jones, and V. Cerundolo, “Biology of CD1- and MR1-restricted T cells,” Annual Review of Immunology, vol. 32, pp. 323–366, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Shamshiev, H.-J. Gober, A. Donda, Z. Mazorra, L. Mori, and G. De Libero, “Presentation of the same glycolipid by different CD1 molecules,” Journal of Experimental Medicine, vol. 195, no. 8, pp. 1013–1021, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. T.-Y. Cheng, M. Relloso, I. Van Rhijn et al., “Role of lipid trimming and CD1 groove size in cellular antigen presentation,” EMBO Journal, vol. 25, no. 13, pp. 2989–2999, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Relloso, T.-Y. Cheng, J. S. Im et al., “pH-Dependent interdomain tethers of CD1b regulate its antigen capture,” Immunity, vol. 28, no. 6, pp. 774–786, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Scharf, N. S. Li, A. J. Hawk et al., “The 2.5 a structure of CD1c in complex with a mycobacterial lipid reveals an open groove ideally suited for diverse antigen presentation,” Immunity, vol. 33, no. 6, pp. 853–862, 2010. View at Publisher · View at Google Scholar
  18. M. Dieudé, H. Striegl, A. J. Tyznik et al., “Cardiolipin binds to CD1d and stimulates CD1d-restricted γδ T cells in the normal murine repertoire,” Journal of Immunology, vol. 186, no. 8, pp. 4771–4781, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. K. S. Wun, G. Cameron, O. Patel et al., “A molecular basis for the exquisite CD1d-restricted antigen specificity and functional responses of natural killer T cells,” Immunity, vol. 34, no. 3, pp. 327–339, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. E. D. Yu, E. Girardi, J. Wang et al., “Structural basis for the recognition of C20:2-αGalCer by the invariant natural killer T cell receptor-like antibody L363,” Journal of Biological Chemistry, vol. 287, no. 2, pp. 1269–1278, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Mallevaey, A. J. Clarke, J. P. Scott-Browne et al., “A molecular basis for NKT cell recognition of CD1d-self-antigen,” Immunity, vol. 34, no. 3, pp. 315–326, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. L. F. Garcia-Alles, G. Giacometti, C. Versluis et al., “Crystal structure of human CD1e reveals a groove suited for lipid-exchange processes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 32, pp. 13230–13235, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. S.-J. Kang and P. Cresswell, “Calnexin, calreticulin, and ERp57 cooperate in disulfide bond formation in human CD1d heavy chain,” The Journal of Biological Chemistry, vol. 277, no. 47, pp. 44838–44844, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Zeissig, S. K. Dougan, D. C. Barral et al., “Primary deficiency of microsomal triglyceride transfer protein in human abetalipoproteinemia is associated with loss of CD1 function,” The Journal of Clinical Investigation, vol. 120, no. 8, pp. 2889–2899, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Kaser, D. L. Hava, S. K. Dougan et al., “Microsomal triglyceride transfer protein regulates endogenous and exogenous antigen presentation by group 1 CD1 molecules,” European Journal of Immunology, vol. 38, no. 8, pp. 2351–2359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. S. K. Dougan, A. Salas, P. Rava et al., “Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells,” The Journal of Experimental Medicine, vol. 202, no. 4, pp. 529–539, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Brozovic, T. Nagaishi, M. Yoshida et al., “CD1d function is regulated by microsomal triglyceride transfer protein,” Nature Medicine, vol. 10, no. 5, pp. 535–539, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Sagiv, L. Bai, D. G. Wei et al., “A distal effect of microsomal triglyceride transfer protein deficiency on the lysosomal recycling of CD1d,” Journal of Experimental Medicine, vol. 204, no. 4, pp. 921–928, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Cox, L. Fox, R. Tian et al., “Determination of cellular lipids bound to human CD1d molecules,” PLoS ONE, vol. 4, no. 5, Article ID 0005325, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Briken, R. M. Jackman, S. Dasgupta, S. Hoening, and S. A. Porcelli, “Intracellular trafficking pathway of newly synthesized CD1b molecules,” The EMBO Journal, vol. 21, no. 4, pp. 825–834, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Sugita, E. P. Grant, E. Van Donselaar et al., “Separate pathways for antigen presentation by CD1 molecules,” Immunity, vol. 11, no. 6, pp. 743–752, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Sugita, N. van Der Wel, R. A. Rogers, P. J. Peters, and M. B. Brenner, “CD1c molecules broadly survey the endocytic system,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 15, pp. 8445–8450, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Sugita, R. M. Jackman, E. Van Donselaar et al., “Cytoplasmic tail-dependent localization of CD1b antigen-presenting molecules to MIICs,” Science, vol. 273, no. 5273, pp. 349–352, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. D. C. Barral, M. Cavallari, P. J. McCormick et al., “CD1a and MHC class I follow a similar endocytic recycling pathway,” Traffic, vol. 9, no. 9, pp. 1446–1457, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Sugita, X. Cao, G. F. M. Watts, R. A. Rogers, J. S. Bonifacino, and M. B. Brenner, “Failure of trafficking and antigen presentation by CD1 in AP-3-deficient cells,” Immunity, vol. 16, no. 5, pp. 697–706, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. Y.-H. Chiu, S.-H. Park, K. Benlagha et al., “Multiple defects in antigen presentation and T cell development by mice expressing cytoplasmic tail-truncated CD1d,” Nature Immunology, vol. 3, no. 1, pp. 55–60, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Jayawardena-Wolf, K. Benlagha, Y.-H. Chiu, R. Mehr, and A. Bendelac, “CD1d endosomal trafficking is independently regulated by an intrinsic CD1d-encoded tyrosine motif and by the invariant chain,” Immunity, vol. 15, no. 6, pp. 897–908, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Sloma, M.-T. Zilber, T. Vasselon et al., “Regulation of CD1a surface expression and antigen presentation by invariant chain and lipid rafts,” The Journal of Immunology, vol. 180, no. 2, pp. 980–987, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. S. Im, P. Arora, G. Bricard et al., “Kinetics and cellular site of glycolipid loading control the outcome of natural killer T cell activation,” Immunity, vol. 30, no. 6, pp. 888–898, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Arora, S. S. Kharkwal, T. W. Ng et al., “Endocytic pH regulates cell surface localization of glycolipid antigen loaded CD1d complexes,” Chemistry and Physics of Lipids, vol. 191, pp. 75–83, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Agea, A. Russano, O. Bistoni et al., “Human CD1-restricted T cell recognition of lipids from pollens,” The Journal of Experimental Medicine, vol. 202, no. 2, pp. 295–308, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. E. Gumperz, C. Roy, A. Makowska et al., “Murine CD1d-restricted T cell recognition of cellular lipids,” Immunity, vol. 12, no. 2, pp. 211–221, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. A. M. Russano, G. Bassotti, E. Agea et al., “CD1-restricted recognition of exogenous and self-lipid antigens by duodenal γδ+ T lymphocytes,” Journal of Immunology, vol. 178, no. 6, pp. 3620–3626, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. I. Van Rhijn, T. Van Berlo, T. Hilmenyuk et al., “Human autoreactive T cells recognize CD1b and phospholipids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 2, pp. 380–385, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. B. J. Wolf, R. V. V. Tatituri, C. F. Almeida et al., “Identification of a potent microbial lipid antigen for diverse NKT cells,” Journal of Immunology, vol. 195, no. 6, pp. 2540–2551, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. R. V. V. Tatituri, G. F. M. Watts, V. Bhowruth et al., “Recognition of microbial and mammalian phospholipid antigens by NKT cells with diverse TCRs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 5, pp. 1827–1832, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Zeissig, K. Murata, L. Sweet et al., “Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity,” Nature Medicine, vol. 18, no. 7, pp. 1060–1068, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. R. W. Birkinshaw, D. G. Pellicci, T.-Y. Cheng et al., “αβ T cell antigen receptor recognition of CD1a presenting self lipid ligands,” Nature Immunology, vol. 16, no. 3, pp. 258–266, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. L. M. Fox, D. G. Cox, J. L. Lockridge et al., “Recognition of lyso-phospholipids by human natural killer T lymphocytes,” PLoS Biology, vol. 7, no. 10, Article ID e1000228, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Blomqvist, S. Rhost, S. Teneberg et al., “Multiple tissue-specific isoforms of sulfatide activate CD1d-restricted type II NKT cells,” European Journal of Immunology, vol. 39, no. 7, pp. 1726–1735, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Shamshiev, A. Donda, T. I. Prigozy et al., “The αβ T cell response to self-glycolipids shows a novel mechanism of CD1b loading and a requirement for complex oligosaccharides,” Immunity, vol. 13, no. 2, pp. 255–264, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. J.-E. Park, D. Y. Wu, M. Prendes et al., “Fine specificity of natural killer T cells against GD3 ganglioside and identification of GM3 as an inhibitory natural killer T-cell ligand,” Immunology, vol. 123, no. 1, pp. 145–155, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Kain, B. Webb, B. L. Anderson et al., “The identification of the endogenous ligands of natural killer t cells reveals the presence of mammalian α-linked glycosylceramides,” Immunity, vol. 41, no. 4, pp. 543–554, 2014. View at Google Scholar
  54. S. Rhost, L. Löfbom, B.-M. Rynmark et al., “Identification of novel glycolipid ligands activating a sulfatide-reactive, CD1d-restricted, type II natural killer T lymphocyte,” European Journal of Immunology, vol. 42, no. 11, pp. 2851–2860, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Nair, C. S. Boddupalli, R. Verma et al., “Type II NKT-TFH cells against Gaucher lipids regulate B-cell immunity and inflammation,” Blood, vol. 125, no. 8, pp. 1256–1271, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Zhou, J. Mattner, C. Cantu III et al., “Lysosomal glycosphingolipid recognition by NKT cells,” Science, vol. 306, no. 5702, pp. 1786–1789, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. X. Long, S. Deng, J. Mattner et al., “Synthesis and evaluation of stimulatory properties of Sphingomonadaceae glycolipids,” Nature Chemical Biology, vol. 3, no. 9, pp. 559–564, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Facciotti, G. S. Ramanjaneyulu, M. Lepore et al., “Peroxisome-derived lipids are self antigens that stimulate invariant natural killer T cells in the thymus,” Nature Immunology, vol. 13, no. 5, pp. 474–480, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Lepore, C. de Lalla, S. R. Gundimeda et al., “A novel self-lipid antigen targets human T cells against CD1c+ leukemias,” Journal of Experimental Medicine, vol. 211, no. 7, pp. 1363–1377, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. A. de Jong, T.-Y. Cheng, S. Huang et al., “CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens,” Nature Immunology, vol. 15, no. 2, pp. 177–185, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. Kinjo, E. Tupin, D. Wu et al., “Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria,” Nature Immunology, vol. 7, no. 9, pp. 978–986, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. D. B. Moody, B. B. Reinhold, M. R. Guy et al., “Structural requirements for glycolipid antigen recognition by CD1b- restricted T cells,” Science, vol. 278, no. 5336, pp. 283–286, 1997. View at Publisher · View at Google Scholar · View at Scopus
  63. P. A. Sieling, D. Chatterjee, S. A. Porcelli et al., “CD1-restricted T cell recognition of microbial lipoglycan antigens,” Science, vol. 269, no. 5221, pp. 227–230, 1995. View at Publisher · View at Google Scholar · View at Scopus
  64. J. L. Amprey, J. S. Im, S. J. Turco et al., “A subset of liver NK T cells is activated during Leishmania donovani infection by CD1d-bound lipophosphoglycan,” Journal of Experimental Medicine, vol. 200, no. 7, pp. 895–904, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. D. B. Moody, D. C. Young, T.-Y. Cheng et al., “T cell activation by lipopeptide antigens,” Science, vol. 303, no. 5657, pp. 527–531, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Ly, A. G. Kasmar, T.-Y. Cheng et al., “CD1c tetramers detect ex vivo T cell responses to processed phosphomycoketide antigens,” Journal of Experimental Medicine, vol. 210, no. 4, pp. 729–741, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. D. B. Moody, T. Ulrichs, W. Mühlecker et al., “CD1c-mediated T-cell recognition of isoprenoid glycolipids in Mycobacterium tuberculosis infection,” Nature, vol. 404, no. 6780, pp. 884–888, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. L. F. Garcia-Alles, A. Collmann, C. Versluis et al., “Structural reorganization of the antigen-binding groove of human CD1b for presentation of mycobacterial sulfoglycolipids,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 43, pp. 17755–17760, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. D. M. Zajonc, M. D. M. Crispin, T. A. Bowden et al., “Molecular mechanism of lipopeptide presentation by CD1a,” Immunity, vol. 22, no. 2, pp. 209–219, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. C. S. Pereira, C. Sa-Miranda, G. De Libero, L. Mori, and M. F. Macedo, “Globotriaosylceramide inhibits iNKT-cell activation in a CD1d-dependent manner,” European Journal of Immunology, vol. 46, no. 1, pp. 147–153, 2016. View at Publisher · View at Google Scholar · View at Scopus
  71. G. De Libero and L. Mori, “Novel insights into lipid antigen presentation,” Trends in Immunology, vol. 33, no. 3, pp. 103–111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Freigang, E. Landais, V. Zadorozhny et al., “Scavenger receptors target glycolipids for natural killer T cell activation,” Journal of Clinical Investigation, vol. 122, no. 11, pp. 3943–3954, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. L. León, R. V. V. Tatituri, R. Grenha et al., “Saposins utilize two strategies for lipid transfer and CD1 antigen presentation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 12, pp. 4357–4364, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. F. Winau, V. Schwierzeck, R. Hurwitz et al., “Saposin C is required for lipid presentation by human CD1b,” Nature Immunology, vol. 5, no. 2, pp. 169–174, 2004. View at Google Scholar
  75. W. Yuan, X. Qi, P. Tsang et al., “Saposin B is the dominant saposin that facilitates lipid binding to human CD1d molecules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 13, pp. 5551–5556, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. M. Salio, H. Ghadbane, O. Dushek et al., “Saposins modulate human invariant natural killer t cells self-Reactivity and facilitate lipid exchange with cd1d molecules during antigen presentation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 49, pp. E4753–E4761, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. S.-J. Kang and P. Cresswell, “Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells,” Nature Immunology, vol. 5, no. 2, pp. 175–181, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. N. Schrantz, Y. Sagiv, Y. Liu, P. B. Savage, A. Bendelac, and L. Teyton, “The Niemann-Pick type C2 protein loads isoglobotrihexosylceramide onto CD1d molecules and contributes to the thymic selection of NKT cells,” Journal of Experimental Medicine, vol. 204, no. 4, pp. 841–852, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Cala-De Paepe, E. Layre, G. Giacometti et al., “Deciphering the role of CD1e protein in mycobacterial phosphatidyl-myo-inositol mannosides (PIM) processing for presentation by CD1b to T lymphocytes,” Journal of Biological Chemistry, vol. 287, no. 37, pp. 31494–31502, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. F. Facciotti, M. Cavallari, C. Angénieux et al., “Fine tuning by human CD1e of lipid-specific immune responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 34, pp. 14228–14233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. D. Zhou, C. Cantu III, Y. Sagiv et al., “Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins,” Science, vol. 303, no. 5657, pp. 523–527, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. D. I. Godfrey, S. Stankovic, and A. G. Baxter, “Raising the NKT cell family,” Nature Immunology, vol. 11, no. 3, pp. 197–206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. C. De Lalla, M. Lepore, F. M. Piccolo et al., “High-frequency and adaptive-like dynamics of human CD1 self-reactive T cells,” European Journal of Immunology, vol. 41, no. 3, pp. 602–610, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Gilleron, S. Stenger, Z. Mazorra et al., “Diacylated sulfoglycolipids are novel mycobacterial antigens stimulating CD1-restricted T cells during infection with Mycobacterium tuberculosis,” The Journal of Experimental Medicine, vol. 199, no. 5, pp. 649–659, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Ulrichs, D. B. Moody, E. Grant, S. H. E. Kaufmann, and S. A. Porcelli, “T-cell responses to CD1-presented lipid antigens in humans with Mycobacterium tuberculosis infection,” Infection and Immunity, vol. 71, no. 6, pp. 3076–3087, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. A. de Jong, V. Peña-Cruz, T.-Y. Cheng, R. A. Clark, I. Van Rhijn, and D. B. Moody, “CD1a-autoreactive T cells are a normal component of the human αβ T cell repertoire,” Nature Immunology, vol. 11, no. 12, pp. 1102–1109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. A. G. Kasmar, I. van Rhijn, T.-Y. Cheng et al., “CD1b tetramers bind αβ T cell receptors to identify a mycobacterial glycolipid-reactive T cell repertoire in humans,” Journal of Experimental Medicine, vol. 208, no. 9, pp. 1741–1747, 2011. View at Publisher · View at Google Scholar · View at Scopus
  88. I. Van Rhijn, A. Kasmar, A. De Jong et al., “A conserved human T cell population targets mycobacterial antigens presented by CD1b,” Nature Immunology, vol. 14, no. 7, pp. 706–713, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. I. Van Rhijn, N. A. Gherardin, A. Kasmar et al., “TCR bias and affinity define two compartments of the CD1b-glycolipid- specific T cell repertoire,” Journal of Immunology, vol. 192, no. 9, pp. 4054–4060, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. S. P. Berzins, M. J. Smyth, and A. G. Baxter, “Presumed guilty: natural killer T cell defects and human disease,” Nature Reviews Immunology, vol. 11, no. 2, pp. 131–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. P. J. Brennan, M. Brigl, and M. B. Brenner, “Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions,” Nature Reviews Immunology, vol. 13, no. 2, pp. 101–117, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. C. J. Montoya, D. Pollard, J. Martinson et al., “Characterization of human invariant natural killer T subsets in health and disease using a novel invariant natural killer T cell-clonotypic monoclonal antibody, 6B11,” Immunology, vol. 122, no. 1, pp. 1–14, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. M. Kanamori, Y. Tasumi, T. Iyoda, M. Ushida, and K. Inaba, “Sulfatide inhibits α-galactosylceramide presentation by dendritic cells,” International Immunology, vol. 24, no. 2, pp. 129–136, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. E. Y. Kim, L. Lynch, P. J. Brennan, N. R. Cohen, and M. B. Brenner, “The transcriptional programs of iNKT cells,” Seminars in Immunology, vol. 27, no. 1, pp. 26–32, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. M. G. Constantinides and A. Bendelac, “Transcriptional regulation of the NKT cell lineage,” Current Opinion in Immunology, vol. 25, no. 2, pp. 161–167, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. P. T. Lee, K. Benlagha, L. Teyton, and A. Bendelac, “Distinct functional lineages of human Vα24 natural killer T cells,” Journal of Experimental Medicine, vol. 195, no. 5, pp. 637–641, 2002. View at Publisher · View at Google Scholar · View at Scopus
  97. J. E. Gumperz, S. Miyake, T. Yamamura, and M. B. Brenner, “Functionally distinct subsets of CD1d-restricted natural killer T cells revealed by CD1d tetramer staining,” Journal of Experimental Medicine, vol. 195, no. 5, pp. 625–636, 2002. View at Publisher · View at Google Scholar · View at Scopus
  98. V. O'Reilly, S. G. Zeng, G. Bricard et al., “Distinct and overlapping effector functions of expanded human CD4+, CD8a+ and CD4−CD8a− invariant natural killer T cells,” PLoS ONE, vol. 6, no. 12, Article ID e28648, 2011. View at Publisher · View at Google Scholar
  99. M.-L. Michel, A. C. Keller, C. Paget et al., “Identification of an IL-17–producing NK1.1neg iNKT cell population involved in airway neutrophilia,” Journal of Experimental Medicine, vol. 204, no. 5, pp. 995–1001, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. J.-M. Doisne, C. Becourt, L. Amniai et al., “Skin and peripheral lymph node invariant NKT cells are mainly retinoic acid receptor-related orphan receptor γt+ and respond preferentially under inflammatory conditions,” The Journal of Immunology, vol. 183, no. 3, pp. 2142–2149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. H. Dai, A. Rahman, A. Saxena et al., “Syndecan-1 identifies and controls the frequency of IL-17-producing naïve natural killer T (NKT17) cells in mice,” European Journal of Immunology, vol. 45, no. 11, pp. 3045–3051, 2015. View at Publisher · View at Google Scholar · View at Scopus
  102. M. Monteiro, C. F. Almeida, A. Agua-Doce, and L. Graca, “Induced IL-17-producing invariant NKT cells require activation in presence of TGF-β and IL-1β,” The Journal of Immunology, vol. 190, no. 2, pp. 805–811, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. M.-L. Michel, D. Mendes-da-Cruz, A. C. Keller et al., “Critical role of ROR-γt in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 50, pp. 19845–19850, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. A. Enders, S. Stankovic, C. Teh et al., “ZBTB7B (Th-POK) regulates the development of IL-17-producing CD1d-restricted mouse NKT cells,” Journal of Immunology, vol. 189, no. 11, pp. 5240–5249, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. I. Engel, M. Zhao, D. Kappes, I. Taniuchi, and M. Kronenberg, “The transcription factor Th-POK negatively regulates Th17 differentiation in Vα14i NKT cells,” Blood, vol. 120, no. 23, pp. 4524–4532, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. T. Hu, H. Wang, A. Simmons et al., “Increased level of E protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets,” The Journal of Immunology, vol. 191, no. 10, pp. 5065–5073, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. T. Takahashi, S. Chiba, M. Nieda et al., “Cutting edge: analysis of human Vα24+CD8+ NKT cells activated by α-galactosylceramide-pulsed monocyte-derived dendritic cells,” Journal of Immunology, vol. 168, no. 7, pp. 3140–3144, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. L. Moreira-Teixeira, M. Resende, M. Coffre et al., “Proinflammatory environment dictates the IL-17-producing capacity of human invariant NKT cells,” Journal of Immunology, vol. 186, no. 10, pp. 5758–5765, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. A. Balreira, M. F. Macedo, C. Girão et al., “Anomalies in conventional T and invariant natural killer T-cell populations in Fabry mice but not in Fabry patients,” British Journal of Haematology, vol. 143, no. 4, pp. 601–604, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. M. F. Macedo, R. Quinta, C. S. Pereira, and M. C. Sa Miranda, “Enzyme replacement therapy partially prevents invariant Natural Killer T cell deficiency in the Fabry disease mouse model,” Molecular Genetics and Metabolism, vol. 106, no. 1, pp. 83–91, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. C. S. Pereira, O. Azevedo, M. L. Maia, A. F. Dias, C. Sa-Miranda, and M. F. Macedo, “Invariant natural killer T cells are phenotypically and functionally altered in Fabry disease,” Molecular Genetics and Metabolism, vol. 108, no. 4, pp. 241–248, 2013. View at Publisher · View at Google Scholar · View at Scopus
  112. I. Marrero, R. Ware, and V. Kumar, “Type II NKT cells in inflammation, autoimmunity, microbial immunity, and cancer,” Frontiers in Immunology, vol. 6, article 316, 2015. View at Publisher · View at Google Scholar · View at Scopus
  113. S. Cardell, S. Tangri, S. Chan, M. Kronenberg, C. Benoist, and D. Mathis, “CD1-restricted CD4+ T cells in major histocompatibility complex class II-deficient mice,” Journal of Experimental Medicine, vol. 182, no. 4, pp. 993–1004, 1995. View at Publisher · View at Google Scholar · View at Scopus
  114. S.-H. Park, A. Weiss, K. Benlagha, T. Kyin, L. Teyton, and A. Bendelac, “The mouse CD1d-restricted repertoire is dominated by a few autoreactive T cell receptor families,” Journal of Experimental Medicine, vol. 193, no. 8, pp. 893–904, 2001. View at Publisher · View at Google Scholar · View at Scopus
  115. J. Zhao, X. Weng, S. Bagchi, and C.-R. Wang, “Polyclonal type II natural killer T cells require PLZF and SAP for their development and contribute to CpG-mediated antitumor response,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 7, pp. 2674–2679, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. L. Bai, D. Picard, B. Anderson et al., “The majority of CD1d-sulfatide-specific T cells in human blood use a semiinvariant Vδ1 TCR,” European Journal of Immunology, vol. 42, no. 9, pp. 2505–2510, 2012. View at Publisher · View at Google Scholar · View at Scopus