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Current Understanding of the Roles of CD1a-Restricted T Cells in the Immune System

  • Yoo, Hyun Jung (Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Na Young (Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Ji Hyung (Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University)
  • Received : 2021.03.14
  • Accepted : 2021.04.01
  • Published : 2021.05.31

Abstract

Cluster of differentiation 1 (CD1) is a family of cell-surface glycoproteins that present lipid antigens to T cells. Humans have five CD1 isoforms. CD1a is distinguished by the small volume of its antigen-binding groove and its stunted A' pocket, its high and exclusive expression on Langerhans cells, and its localization in the early endosomal and recycling intracellular trafficking compartments. Its ligands originate from self or foreign sources. There are three modes by which the T-cell receptors of CD1a-restricted T cells interact with the CD1a:lipid complex: they bind to both the CD1a surface and the antigen or to only CD1a itself, which activates the T cell, or they are unable to bind because of bulky motifs protruding from the antigen-binding groove, which might inhibit autoreactive T-cell activation. Recently, several studies have shown that by producing TH2 or TH17 cytokines, CD1a-restricted T cells contribute to inflammatory skin disorders, including atopic dermatitis, psoriasis, allergic contact dermatitis, and wasp/bee venom allergy. They may also participate in other diseases, including pulmonary disorders and cancer, because CD1a-expressing dendritic cells are also located in non-skin tissues. In this mini-review, we discuss the current knowledge regarding the biology of CD1a-reactive T cells and their potential roles in disease.

Keywords

Acknowledgement

This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2018R1D1A1B07048813) and Korea University Grant K1807481.

References

  1. Agea, E., Russano, A., Bistoni, O., Mannucci, R., Nicoletti, I., Corazzi, L., Postle, A.D., De Libero, G., Porcelli, S.A., and Spinozzi, F. (2005). Human CD1-restricted T cell recognition of lipids from pollens. J. Exp. Med. 202, 295-308. https://doi.org/10.1084/jem.20050773
  2. Akbari, O., Stock, P., Meyer, E., Kronenberg, M., Sidobre, S., Nakayama, T., Taniguchi, M., Grusby, M.J., DeKruyff, R.H., and Umetsu, D.T. (2003). Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat. Med. 9, 582-588. https://doi.org/10.1038/nm851
  3. Angenieux, C., Salamero, J., Fricker, D., Cazenave, J.P., Goud, B., Hanau, D., and de La Salle, H. (2000). Characterization of CD1e, a third type of CD1 molecule expressed in dendritic cells. J. Biol. Chem. 275, 37757-37764. https://doi.org/10.1074/jbc.M007082200
  4. Baharom, F., Thomas, S., Rankin, G., Lepzien, R., Pourazar, J., Behndig, A.F., Ahlm, C., Blomberg, A., and Smed-Sorensen, A. (2016). Dendritic cells and monocytes with distinct inflammatory responses reside in lung mucosa of healthy humans. J. Immunol. 196, 4498-4509. https://doi.org/10.4049/jimmunol.1600071
  5. Balato, A., Lembo, S., Mattii, M., Schiattarella, M., Marino, R., De Paulis, A., Balato, N., and Ayala, F. (2012). IL-33 is secreted by psoriatic keratinocytes and induces pro-inflammatory cytokines via keratinocyte and mast cell activation. Exp. Dermatol. 21, 892-894. https://doi.org/10.1111/exd.12027
  6. Barral, D.C., Cavallari, M., McCormick, P.J., Garg, S., Magee, A.I., Bonifacino, J.S., De Libero, G., and Brenner, M.B. (2008). CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 9, 1446-1457. https://doi.org/10.1111/j.1600-0854.2008.00781.x
  7. Beckman, E.M., Porcelli, S.A., Morita, C.T., Behar, S.M., Furlong, S.T., and Brenner, M.B. (1994). Recognition of a lipid antigen by CD1-restricted αβ+ T cells. Nature 372, 691-694. https://doi.org/10.1038/372691a0
  8. Benlagha, K., Weiss, A., Beavis, A., Teyton, L., and Bendelac, A. (2000). In vivo identification of glycolipid antigen-specific T cells using fluorescent CD1d tetramers. J. Exp. Med. 191, 1895-1903. https://doi.org/10.1084/jem.191.11.1895
  9. Bertorelli, G., Bocchino, V., Zhou, X., Zanini, A., Bernini, M.V., Damia, R., Di Comite, V., Grima, P., and Olivieri, D. (2000). Dendritic cell number is related to IL-4 expression in the airways of atopic asthmatic subjects. Allergy 55, 449-454. https://doi.org/10.1034/j.1398-9995.2000.055005449.x
  10. Betts, R.J., Perkovic, A., Mahapatra, S., Del Bufalo, A., Camara, K., Howell, A.R., Martinozzi Teissier, S., De Libero, G., and Mori, L. (2017). Contact sensitizers trigger human CD1-autoreactive T-cell responses. Eur. J. Immunol. 47, 1171-1180. https://doi.org/10.1002/eji.201746939
  11. Birkinshaw, R.W., Pellicci, D.G., Cheng, T.Y., Keller, A.N., Sandoval-Romero, M., Gras, S., de Jong, A., Uldrich, A.P., Moody, D.B., Godfrey, D.I., et al. (2015). αβ T cell antigen receptor recognition of CD1a presenting self lipid ligands. Nat. Immunol. 16, 258-266. https://doi.org/10.1038/ni.3098
  12. Bourgeois, E.A., Subramaniam, S., Cheng, T.Y., De Jong, A., Layre, E., Ly, D., Salimi, M., Legaspi, A., Modlin, R.L., Salio, M., et al. (2015). Bee venom processes human skin lipids for presentation by CD1a. J. Exp. Med. 212, 149-163. https://doi.org/10.1084/jem.20141505
  13. Briken, V., Jackman, R.M., Dasgupta, S., Hoening, S., and Porcelli, S.A. (2002). Intracellular trafficking pathway of newly synthesized CD1b molecules. EMBO J. 21, 825-834. https://doi.org/10.1093/emboj/21.4.825
  14. Briken, V., Jackman, R.M., Watts, G.F., Rogers, R.A., and Porcelli, S.A. (2000). Human CD1b and CD1c isoforms survey different intracellular compartments for the presentation of microbial lipid antigens. J. Exp. Med. 192, 281-288. https://doi.org/10.1084/jem.192.2.281
  15. Calabi, F., Jarvis, J.M., Martin, L., and Milstein, C. (1989). Two classes of CD1 genes. Eur. J. Immunol. 19, 285-292. https://doi.org/10.1002/eji.1830190211
  16. Carbone, F.R. and Gleeson, P.A. (1997). Carbohydrates and antigen recognition by T cells. Glycobiology 7, 725-730. https://doi.org/10.1093/glycob/7.6.725-d
  17. Cernadas, M., Cavallari, M., Watts, G., Mori, L., De Libero, G., and Brenner, M.B. (2010). Early recycling compartment trafficking of CD1a is essential for its intersection and presentation of lipid antigens. J. Immunol. 184, 1235-1241. https://doi.org/10.4049/jimmunol.0804140
  18. Cheung, K.L., Jarrett, R., Subramaniam, S., Salimi, M., Gutowska-Owsiak, D., Chen, Y.L., Hardman, C., Xue, L., Cerundolo, V., and Ogg, G. (2016). Psoriatic T cells recognize neolipid antigens generated by mast cell phospholipase delivered by exosomes and presented by CD1a. J. Exp. Med. 213, 2399-2412. https://doi.org/10.1084/jem.20160258
  19. Corbett, A.J., Eckle, S.B., Birkinshaw, R.W., Liu, L., Patel, O., Mahony, J., Chen, Z., Reantragoon, R., Meehan, B., Cao, H., et al. (2014). T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509, 361-365. https://doi.org/10.1038/nature13160
  20. Cotton, R.N., Cheng, T.Y., Wegrecki, M., Le Nours, J., Orgill, D.P., Pomahac, B., Talbot, S.G., Willis, R.A., Altman, J.D., de Jong, A., et al. (2021). Human skin is colonized by T cells that recognize CD1a independently of lipid. J. Clin. Invest. 131, e140706. https://doi.org/10.1172/JCI140706
  21. de Jong, A., Cheng, T.Y., Huang, S., Gras, S., Birkinshaw, R.W., Kasmar, A.G., Van Rhijn, I., Pena-Cruz, V., Ruan, D.T., Altman, J.D., et al. (2014). CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens. Nat. Immunol. 15, 177-185. https://doi.org/10.1038/ni.2790
  22. de Jong, A., Pena-Cruz, V., Cheng, T.Y., Clark, R.A., Van Rhijn, I., and Moody, D.B. (2010). CD1a-autoreactive T cells are a normal component of the human αβ T cell repertoire. Nat. Immunol. 11, 1102-1109. https://doi.org/10.1038/ni.1956
  23. de Lalla, C., Lepore, M., Piccolo, F.M., Rinaldi, A., Scelfo, A., Garavaglia, C., Mori, L., De Libero, G., Dellabona, P., and Casorati, G. (2011). High-frequency and adaptive-like dynamics of human CD1 self-reactive T cells. Eur. J. Immunol. 41, 602-610. https://doi.org/10.1002/eji.201041211
  24. Facciotti, F., Cavallari, M., Angenieux, C., Garcia-Alles, L.F., Signorino-Gelo, F., Angman, L., Gilleron, M., Prandi, J., Puzo, G., Panza, L., et al. (2011). Fine tuning by human CD1e of lipid-specific immune responses. Proc. Natl. Acad. Sci. U. S. A. 108, 14228-14233. https://doi.org/10.1073/pnas.1108809108
  25. Gadola, S.D., Zaccai, N.R., Harlos, K., Shepherd, D., Castro-Palomino, J.C., Ritter, G., Schmidt, R.R., Jones, E.Y., and Cerundolo, V. (2002). Structure of human CD1b with bound ligands at 2.3 Å, a maze for alkyl chains. Nat. Immunol. 3, 721-726. https://doi.org/10.1038/ni821
  26. Gamerdinger, K., Moulon, C., Karp, D.R., Van Bergen, J., Koning, F., Wild, D., Pflugfelder, U., and Weltzien, H.U. (2003). A new type of metal recognition by human T cells: contact residues for peptide-independent bridging of T cell receptor and major histocompatibility complex by nickel. J. Exp. Med. 197, 1345-1353. https://doi.org/10.1084/jem.20030121
  27. Han, M., Hannick, L.I., DiBrino, M., and Robinson, M.A. (1999). Polymorphism of human CD1 genes. Tissue Antigens 54, 122-127. https://doi.org/10.1034/j.1399-0039.1999.540202.x
  28. Haniffa, M., Shin, A., Bigley, V., McGovern, N., Teo, P., See, P., Wasan, P.S., Wang, X.N., Malinarich, F., Malleret, B., et al. (2012). Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 37, 60-73. https://doi.org/10.1016/j.immuni.2012.04.012
  29. Hardman, C.S., Chen, Y.L., Salimi, M., Jarrett, R., Johnson, D., Jarvinen, V.J., Owens, R.J., Repapi, E., Cousins, D.J., Barlow, J.L., et al. (2017). CD1a presentation of endogenous antigens by group 2 innate lymphoid cells. Sci. Immunol. 2, eaan5918. https://doi.org/10.1126/sciimmunol.aan5918
  30. Jarrett, R., Salio, M., Lloyd-Lavery, A., Subramaniam, S., Bourgeois, E., Archer, C., Cheung, K.L., Hardman, C., Chandler, D., Salimi, M., et al. (2016). Filaggrin inhibits generation of CD1a neolipid antigens by house dust mite-derived phospholipase. Sci. Transl. Med. 8, 325ra318.
  31. Kagami, S., Rizzo, H.L., Lee, J.J., Koguchi, Y., and Blauvelt, A. (2010). Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J. Invest. Dermatol. 130, 1373-1383. https://doi.org/10.1038/jid.2009.399
  32. Kai, K., Tanaka, T., Ide, T., Kawaguchi, A., Noshiro, H., and Aishima, S. (2021). Immunohistochemical analysis of the aggregation of CD1a-positive dendritic cells in resected specimens and its association with surgical outcomes for patients with gallbladder cancer. Transl. Oncol. 14, 100923. https://doi.org/10.1016/j.tranon.2020.100923
  33. Kaplan, D.H., Igyarto, B.Z., and Gaspari, A.A. (2012). Early immune events in the induction of allergic contact dermatitis. Nat. Rev. Immunol. 12, 114-124. https://doi.org/10.1038/nri3150
  34. Kasmar, A.G., Van Rhijn, I., Magalhaes, K.G., Young, D.C., Cheng, T.Y., Turner, M.T., Schiefner, A., Kalathur, R.C., Wilson, I.A., Bhati, M., et al. (2013). Cutting Edge: CD1a tetramers and dextramers identify human lipopeptide-specific T cells ex vivo. J. Immunol. 191, 4499-4503. https://doi.org/10.4049/jimmunol.1301660
  35. Kawano, T., Cui, J., Koezuka, Y., Toura, I., Kaneko, Y., Motoki, K., Ueno, H., Nakagawa, R., Sato, H., Kondo, E., et al. (1997). CD1d-restricted and TCR-mediated activation of vα14 NKT cells by glycosylceramides. Science 278, 1626-1629. https://doi.org/10.1126/science.278.5343.1626
  36. Kim, J.H., Hu, Y., Yongqing, T., Kim, J., Hughes, V.A., Le Nours, J., Marquez, E.A., Purcell, A.W., Wan, Q., Sugita, M., et al. (2016). CD1a on Langerhans cells controls inflammatory skin disease. Nat. Immunol. 17, 1159-1166. https://doi.org/10.1038/ni.3523
  37. Kinjo, Y., Tupin, E., Wu, D., Fujio, M., Garcia-Navarro, R., Benhnia, M.R., Zajonc, D.M., Ben-Menachem, G., Ainge, G.D., Painter, G.F., et al. (2006). Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat. Immunol. 7, 978-986. https://doi.org/10.1038/ni1380
  38. Kjer-Nielsen, L., Patel, O., Corbett, A.J., Le Nours, J., Meehan, B., Liu, L., Bhati, M., Chen, Z., Kostenko, L., Reantragoon, R., et al. (2012). MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491, 717-723. https://doi.org/10.1038/nature11605
  39. Lepore, M., de Lalla, C., Gundimeda, S.R., Gsellinger, H., Consonni, M., Garavaglia, C., Sansano, S., Piccolo, F., Scelfo, A., Haussinger, D., et al. (2014). A novel self-lipid antigen targets human T cells against CD1c+ leukemias. J. Exp. Med. 211, 1363-1377. https://doi.org/10.1084/jem.20140410
  40. Manolova, V., Kistowska, M., Paoletti, S., Baltariu, G.M., Bausinger, H., Hanau, D., Mori, L., and De Libero, G. (2006). Functional CD1a is stabilized by exogenous lipids. Eur. J. Immunol. 36, 1083-1092. https://doi.org/10.1002/eji.200535544
  41. Matsuda, J.L., Naidenko, O.V., Gapin, L., Nakayama, T., Taniguchi, M., Wang, C.R., Koezuka, Y., and Kronenberg, M. (2000). Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J. Exp. Med. 192, 741-754. https://doi.org/10.1084/jem.192.5.741
  42. Miller, C.J., McChesney, M., and Moore, P.F. (1992). Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Lab. Invest. 67, 628-634.
  43. Moody, D.B., Young, D.C., Cheng, T.Y., Rosat, J.P., Roura-Mir, C., O'Connor, P.B., Zajonc, D.M., Walz, A., Miller, M.J., Levery, S.B., et al. (2004). T cell activation by lipopeptide antigens. Science 303, 527-531. https://doi.org/10.1126/science.1089353
  44. Nestle, F.O., Conrad, C., Tun-Kyi, A., Homey, B., Gombert, M., Boyman, O., Burg, G., Liu, Y.J., and Gilliet, M. (2005). Plasmacytoid predendritic cells initiate psoriasis through interferon-α production. J. Exp. Med. 202, 135-143. https://doi.org/10.1084/jem.20050500
  45. Nicolai, S., Wegrecki, M., Cheng, T.Y., Bourgeois, E.A., Cotton, R.N., Mayfield, J.A., Monnot, G.C., Le Nours, J., Van Rhijn, I., Rossjohn, J., et al. (2020). Human T cell response to CD1a and contact dermatitis allergens in botanical extracts and commercial skin care products. Sci. Immunol. 5, eaax5430. https://doi.org/10.1126/sciimmunol.aax5430
  46. Park, S.H., Weiss, A., Benlagha, K., Kyin, T., Teyton, L., and Bendelac, A. (2001). The mouse CD1d-restricted repertoire is dominated by a few autoreactive T cell receptor families. J. Exp. Med. 193, 893-904. https://doi.org/10.1084/jem.193.8.893
  47. Porcelli, S., Brenner, M.B., Greenstein, J.L., Balk, S.P., Terhorst, C., and Bleicher, P.A. (1989). Recognition of cluster of differentiation 1 antigens by human CD4-CD8- cytolytic T lymphocytes. Nature 341, 447-450. https://doi.org/10.1038/341447a0
  48. Radwan, J., Babik, W., Kaufman, J., Lenz, T.L., and Winternitz, J. (2020). Advances in the evolutionary understanding of MHC polymorphism. Trends Genet. 36, 298-311. https://doi.org/10.1016/j.tig.2020.01.008
  49. Raftery, M.J., Hitzler, M., Winau, F., Giese, T., Plachter, B., Kaufmann, S.H., and Schonrich, G. (2008). Inhibition of CD1 antigen presentation by human cytomegalovirus. J. Virol. 82, 4308-4319. https://doi.org/10.1128/JVI.01447-07
  50. Rosat, J.P., Grant, E.P., Beckman, E.M., Dascher, C.C., Sieling, P.A., Frederique, D., Modlin, R.L., Porcelli, S.A., Furlong, S.T., and Brenner, M.B. (1999). CD1-restricted microbial lipid antigen-specific recognition found in the CD8+ αβ T cell pool. J. Immunol. 162, 366-371.
  51. Salimi, M., Barlow, J.L., Saunders, S.P., Xue, L., Gutowska-Owsiak, D., Wang, X., Huang, L.C., Johnson, D., Scanlon, S.T., McKenzie, A.N., et al. (2013). A role for IL-25 and IL-33-driven type-2 innate lymphoid cells in atopic dermatitis. J. Exp. Med. 210, 2939-2950. https://doi.org/10.1084/jem.20130351
  52. Sandel, M.H., Dadabayev, A.R., Menon, A.G., Morreau, H., Melief, C.J., Offringa, R., van der Burg, S.H., Janssen-van Rhijn, C.M., Ensink, N.G., Tollenaar, R.A., et al. (2005). Prognostic value of tumor-infiltrating dendritic cells in colorectal cancer: role of maturation status and intratumoral localization. Clin. Cancer Res. 11, 2576-2582. https://doi.org/10.1158/1078-0432.CCR-04-1448
  53. Scharf, L., Li, N.S., Hawk, A.J., Garzon, D., Zhang, T., Fox, L.M., Kazen, A.R., Shah, S., Haddadian, E.J., Gumperz, J.E., et al. (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, 853-862. https://doi.org/10.1016/j.immuni.2010.11.026
  54. Schnellhardt, S., Erber, R., Buttner-Herold, M., Rosahl, M.C., Ott, O.J., Strnad, V., Beckmann, M.W., King, L., Hartmann, A., Fietkau, R., et al. (2020). Tumour-infiltrating inflammatory cells in early breast cancer: an underrated prognostic and predictive factor? Int. J. Mol. Sci. 21, 8238. https://doi.org/10.3390/ijms21218238
  55. Seshadri, C., Shenoy, M., Wells, R.D., Hensley-McBain, T., Andersen-Nissen, E., McElrath, M.J., Cheng, T.Y., Moody, D.B., and Hawn, T.R. (2013). Human CD1a deficiency is common and genetically regulated. J. Immunol. 191, 1586-1593. https://doi.org/10.4049/jimmunol.1300575
  56. Shamshiev, A., Gober, H.J., Donda, A., Mazorra, Z., Mori, L., and De Libero, G. (2002). Presentation of the same glycolipid by different CD1 molecules. J. Exp. Med. 195, 1013-1021. https://doi.org/10.1084/jem.20011963
  57. Sharma, M., Zhang, X., Zhang, S., Niu, L., Ho, S.M., Chen, A., and Huang, S. (2017). Inhibition of endocytic lipid antigen presentation by common lipophilic environmental pollutants. Sci. Rep. 7, 2085. https://doi.org/10.1038/s41598-017-02229-7
  58. Sieling, P.A., Torrelles, J.B., Stenger, S., Chung, W., Burdick, A.E., Rea, T.H., Brennan, P.J., Belisle, J.T., Porcelli, S.A., and Modlin, R.L. (2005). The human CD1-restricted T cell repertoire is limited to cross-reactive antigens: implications for host responses against immunologically related pathogens. J. Immunol. 174, 2637-2644. https://doi.org/10.4049/jimmunol.174.5.2637
  59. Subramaniam, S., Aslam, A., Misbah, S.A., Salio, M., Cerundolo, V., Moody, D.B., and Ogg, G. (2016). Elevated and cross-responsive CD1a-reactive T cells in bee and wasp venom allergic individuals. Eur. J. Immunol. 46, 242-252. https://doi.org/10.1002/eji.201545869
  60. Sugita, M., Cao, X., Watts, G.F., Rogers, R.A., Bonifacino, J.S., and Brenner, M.B. (2002). Failure of trafficking and antigen presentation by CD1 in AP-3-deficient cells. Immunity 16, 697-706. https://doi.org/10.1016/S1074-7613(02)00311-4
  61. Sugita, M., Grant, E.P., van Donselaar, E., Hsu, V.W., Rogers, R.A., Peters, P.J., and Brenner, M.B. (1999). Separate pathways for antigen presentation by CD1 molecules. Immunity 11, 743-752. https://doi.org/10.1016/S1074-7613(00)80148-X
  62. Sugita, M., Porcelli, S.A., and Brenner, M.B. (1997). Assembly and retention of CD1b heavy chains in the endoplasmic reticulum. J. Immunol. 159, 2358-2365.
  63. Sugita, M., van Der Wel, N., Rogers, R.A., Peters, P.J., and Brenner, M.B. (2000). CD1c molecules broadly survey the endocytic system. Proc. Natl. Acad. Sci. U. S. A. 97, 8445-8450. https://doi.org/10.1073/pnas.150236797
  64. Suzuki, A., Masuda, A., Nagata, H., Kameoka, S., Kikawada, Y., Yamakawa, M., and Kasajima, T. (2002). Mature dendritic cells make clusters with T cells in the invasive margin of colorectal carcinoma. J. Pathol. 196, 37-43. https://doi.org/10.1002/path.1018
  65. Tazi, A., Bouchonnet, F., Grandsaigne, M., Boumsell, L., Hance, A.J., and Soler, P. (1993). Evidence that granulocyte macrophage-colony-stimulating factor regulates the distribution and differentiated state of dendritic cells/Langerhans cells in human lung and lung cancers. J. Clin. Invest. 91, 566-576. https://doi.org/10.1172/JCI116236
  66. Vasquez, A.M., Mouchlis, V.D., and Dennis, E.A. (2018). Review of four major distinct types of human phospholipase A2. Adv. Biol. Regul. 67, 212-218. https://doi.org/10.1016/j.jbior.2017.10.009
  67. Visvabharathy, L., Genardi, S., Cao, L., He, Y., Alonzo, F., 3rd, Berdyshev, E., and Wang, C.R. (2020). Group 1 CD1-restricted T cells contribute to control of systemic Staphylococcus aureus infection. PLoS Pathog. 16, e1008443. https://doi.org/10.1371/journal.ppat.1008443
  68. Vocanson, M., Hennino, A., Rozieres, A., Poyet, G., and Nicolas, J.F. (2009). Effector and regulatory mechanisms in allergic contact dermatitis. Allergy 64, 1699-1714. https://doi.org/10.1111/j.1398-9995.2009.02082.x
  69. Wollenberg, A., Kraft, S., Hanau, D., and Bieber, T. (1996). Immuno-morphological and ultrastructural characterization of Langerhans cells and a novel, inflammatory dendritic epidermal cell (IDEC) population in lesional skin of atopic eczema. J. Invest. Dermatol. 106, 446-453. https://doi.org/10.1111/1523-1747.ep12343596
  70. Yoshida, A., Imayama, S., Sugai, S., Kawano, Y., and Ishibashi, T. (1997). Increased number of IgE positive Langerhans cells in the conjunctiva of patients with atopic dermatitis. Br. J. Ophthalmol. 81, 402-406. https://doi.org/10.1136/bjo.81.5.402
  71. Zajonc, D.M., Crispin, M.D., Bowden, T.A., Young, D.C., Cheng, T.Y., Hu, J., Costello, C.E., Rudd, P.M., Dwek, R.A., Miller, M.J., et al. (2005). Molecular mechanism of lipopeptide presentation by CD1a. Immunity 22, 209-219. https://doi.org/10.1016/j.immuni.2004.12.009
  72. Zajonc, D.M., Elsliger, M.A., Teyton, L., and Wilson, I.A. (2003). Crystal structure of CD1a in complex with a sulfatide self antigen at a resolution of 2.15 Å. Nat. Immunol. 4, 808-815. https://doi.org/10.1038/ni948
  73. Zeng, Z., Castano, A.R., Segelke, B.W., Stura, E.A., Peterson, P.A., and Wilson, I.A. (1997). Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277, 339-345. https://doi.org/10.1126/science.277.5324.339

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