1zhn Citations

Crystal structure of mouse CD1d bound to the self ligand phosphatidylcholine: a molecular basis for NKT cell activation.

Abstract

NKT cells are immunoregulatory lymphocytes whose activation is triggered by the recognition of lipid Ags in the context of the CD1d molecules by the TCR. In this study we present the crystal structure to 2.8 A of mouse CD1d bound to phosphatidylcholine. The interactions between the ligand acyl chains and the CD1d molecule define the structural and chemical requirements for the binding of lipid Ags to CD1d. The orientation of the polar headgroup toward the C terminus of the alpha1 helix provides a rationale for the structural basis for the observed Valpha chain bias in invariant NKT cells. The contribution of the ligand to the protein surface suggests a likely mode of recognition of lipid Ags by the NKT cell TCR.

Reviews - 1zhn mentioned but not cited (2)

  1. NKT cell ligand recognition logic: molecular basis for a synaptic duet and transmission of inflammatory effectors. Joyce S, Girardi E, Zajonc DM. J Immunol 187 1081-1089 (2011)
  2. Presentation of lipid antigens by CD1 glycoproteins. Schiefner A, Wilson IA. Curr Pharm Des 15 3311-3317 (2009)

Articles - 1zhn mentioned but not cited (4)

  1. Structure and binding kinetics of three different human CD1d-alpha-galactosylceramide-specific T cell receptors. Gadola SD, Koch M, Marles-Wright J, Lissin NM, Shepherd D, Matulis G, Harlos K, Villiger PM, Stuart DI, Jakobsen BK, Cerundolo V, Jones EY. J Exp Med 203 699-710 (2006)
  2. Lysophospholipid presentation by CD1d and recognition by a human Natural Killer T-cell receptor. López-Sagaseta J, Sibener LV, Kung JE, Gumperz J, Adams EJ. EMBO J 31 2047-2059 (2012)
  3. Differing roles of CD1d2 and CD1d1 proteins in type I natural killer T cell development and function. Sundararaj S, Zhang J, Krovi SH, Bedel R, Tuttle KD, Veerapen N, Besra GS, Khandokar Y, Praveena T, Le Nours J, Matsuda JL, Rossjohn J, Gapin L. Proc Natl Acad Sci U S A 115 E1204-E1213 (2018)
  4. What one lipid giveth, another taketh away. Joyce S, Spiller BW, Van Kaer L. Nat Immunol 20 1559-1561 (2019)


Reviews citing this publication (40)

  1. The role of NKT cells in tumor immunity. Terabe M, Berzofsky JA. Adv Cancer Res 101 277-348 (2008)
  2. Evolutionarily conserved amino acids that control TCR-MHC interaction. Marrack P, Scott-Browne JP, Dai S, Gapin L, Kappler JW. Annu Rev Immunol 26 171-203 (2008)
  3. Biology of CD1- and MR1-restricted T cells. Salio M, Silk JD, Jones EY, Cerundolo V. Annu Rev Immunol 32 323-366 (2014)
  4. CD1d ligands: the good, the bad, and the ugly. Brutkiewicz RR. J Immunol 177 769-775 (2006)
  5. The fidelity, occasional promiscuity, and versatility of T cell receptor recognition. Godfrey DI, Rossjohn J, McCluskey J. Immunity 28 304-314 (2008)
  6. How invariant natural killer T cells respond to infection by recognizing microbial or endogenous lipid antigens. Brigl M, Brenner MB. Semin Immunol 22 79-86 (2010)
  7. Antigen recognition by CD1d-restricted NKT T cell receptors. Godfrey DI, Pellicci DG, Patel O, Kjer-Nielsen L, McCluskey J, Rossjohn J. Semin Immunol 22 61-67 (2010)
  8. Microsomal triglyceride transfer protein in plasma and cellular lipid metabolism. Hussain MM, Rava P, Pan X, Dai K, Dougan SK, Iqbal J, Lazare F, Khatun I. Curr Opin Lipidol 19 277-284 (2008)
  9. Therapeutic manipulation of natural killer (NK) T cells in autoimmunity: are we close to reality? Simoni Y, Diana J, Ghazarian L, Beaudoin L, Lehuen A. Clin Exp Immunol 171 8-19 (2013)
  10. Glycolipids as immunostimulating agents. Wu D, Fujio M, Wong CH. Bioorg Med Chem 16 1073-1083 (2008)
  11. Role of Innate T Cells in Anti-Bacterial Immunity. Gao Y, Williams AP. Front Immunol 6 302 (2015)
  12. Natural killer T cells and the regulation of asthma. Matangkasombut P, Pichavant M, Dekruyff RH, Umetsu DT. Mucosal Immunol 2 383-392 (2009)
  13. Phosphatidylcholine-Derived Lipid Mediators: The Crosstalk Between Cancer Cells and Immune Cells. Saito RF, Andrade LNS, Bustos SO, Chammas R. Front Immunol 13 768606 (2022)
  14. CD1 mediated T cell recognition of glycolipids. Zajonc DM, Kronenberg M. Curr Opin Struct Biol 17 521-529 (2007)
  15. Recognition of Microbial Glycolipids by Natural Killer T Cells. Zajonc DM, Girardi E. Front Immunol 6 400 (2015)
  16. Structural and functional aspects of lipid binding by CD1 molecules. Silk JD, Salio M, Brown J, Jones EY, Cerundolo V. Annu Rev Cell Dev Biol 24 369-395 (2008)
  17. TLR gateways to CD1 function. Moody DB. Nat Immunol 7 811-817 (2006)
  18. Role of Group 1 CD1-Restricted T Cells in Infectious Disease. Siddiqui S, Visvabharathy L, Wang CR. Front Immunol 6 337 (2015)
  19. T-cell recognition of glycolipids presented by CD1 proteins. Young DC, Moody DB. Glycobiology 16 103R-112R (2006)
  20. Carbohydrate specificity of the recognition of diverse glycolipids by natural killer T cells. Zajonc DM, Kronenberg M. Immunol Rev 230 188-200 (2009)
  21. Phospholipid--driven gene regulation. Musille PM, Kohn JA, Ortlund EA. FEBS Lett 587 1238-1246 (2013)
  22. Strategy of lipid recognition by invariant natural killer T cells: 'one for all and all for one'. Mallevaey T, Selvanantham T. Immunology 136 273-282 (2012)
  23. Tailored design of NKT-stimulatory glycolipids for polarization of immune responses. Hung JT, Huang JR, Yu AL. J Biomed Sci 24 22 (2017)
  24. Glucocerebroside: an evolutionary advantage for patients with Gaucher disease and a new immunomodulatory agent. Ilan Y, Elstein D, Zimran A. Immunol Cell Biol 87 514-524 (2009)
  25. NKT cells in cardiovascular diseases. van Puijvelde GHM, Kuiper J. Eur J Pharmacol 816 47-57 (2017)
  26. A closer look at CD1d molecules: new horizons in studying NKT cells. Stronge VS, Salio M, Jones EY, Cerundolo V. Trends Immunol 28 455-462 (2007)
  27. Raising the roof: the preferential pharmacological stimulation of Th1 and th2 responses mediated by NKT cells. East JE, Kennedy AJ, Webb TJ. Med Res Rev 34 45-76 (2014)
  28. CD1d presentation of glycolipids. Speak AO, Cerundolo V, Platt FM. Immunol Cell Biol 86 588-597 (2008)
  29. The versatility of the αβ T-cell antigen receptor. Bhati M, Cole DK, McCluskey J, Sewell AK, Rossjohn J. Protein Sci 23 260-272 (2014)
  30. CD1d-restricted glycolipid antigens: presentation principles, recognition logic and functional consequences. Florence WC, Bhat RK, Joyce S. Expert Rev Mol Med 10 e20 (2008)
  31. Mechanisms of lipid-antigen generation and presentation to T cells. De Libero G, Mori L. Trends Immunol 27 485-492 (2006)
  32. Presentation of lipid antigens to T cells. Mori L, De Libero G. Immunol Lett 117 1-8 (2008)
  33. The cellular and biochemical rules of lipid antigen presentation. De Libero G, Collmann A, Mori L. Eur J Immunol 39 2648-2656 (2009)
  34. The CD1 family: serving lipid antigens to T cells since the Mesozoic era. Zajonc DM. Immunogenetics 68 561-576 (2016)
  35. Group 1 CD1-restricted T cells and the pathophysiological implications of self-lipid antigen recognition. Dellabona P, Consonni M, de Lalla C, Casorati G. Tissue Antigens 86 393-405 (2015)
  36. Immunosuppressive roles of natural killer T (NKT) cells in the skin. McKee SJ, Mattarollo SR, Leggatt GR. J Leukoc Biol 96 49-54 (2014)
  37. How T lymphocytes recognize lipid antigens. De Libero G, Mori L. FEBS Lett 580 5580-5587 (2006)
  38. beta-Glycosphingolipids as immune modulators. Adar T, Ilan Y. J Immunotoxicol 5 209-220 (2008)
  39. How T cells get grip on lipid antigens. De Libero G, Mori L. Curr Opin Immunol 20 96-104 (2008)
  40. Invariant natural killer cells in the response to bacteria: the advent of specific antigens. Wingender G, Kronenberg M. Future Microbiol 1 325-340 (2006)

Articles citing this publication (40)

  1. The length of lipids bound to human CD1d molecules modulates the affinity of NKT cell TCR and the threshold of NKT cell activation. 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. J Exp Med 204 1131-1144 (2007)
  2. Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity. Zajonc DM, Maricic I, Wu D, Halder R, Roy K, Wong CH, Kumar V, Wilson IA. J Exp Med 202 1517-1526 (2005)
  3. Inflammation-associated lysophospholipids as ligands for CD1d-restricted T cells in human cancer. Chang DH, Deng H, Matthews P, Krasovsky J, Ragupathi G, Spisek R, Mazumder A, Vesole DH, Jagannath S, Dhodapkar MV. Blood 112 1308-1316 (2008)
  4. Determination of cellular lipids bound to human CD1d molecules. Cox D, Fox L, Tian R, Bardet W, Skaley M, Mojsilovic D, Gumperz J, Hildebrand W. PLoS One 4 e5325 (2009)
  5. A molecular basis for NKT cell recognition of CD1d-self-antigen. 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. Immunity 34 315-326 (2011)
  6. Design of natural killer T cell activators: structure and function of a microbial glycosphingolipid bound to mouse CD1d. Wu D, Zajonc DM, Fujio M, Sullivan BA, Kinjo Y, Kronenberg M, Wilson IA, Wong CH. Proc Natl Acad Sci U S A 103 3972-3977 (2006)
  7. Cardiolipin binds to CD1d and stimulates CD1d-restricted γδ T cells in the normal murine repertoire. Dieudé M, Striegl H, Tyznik AJ, Wang J, Behar SM, Piccirillo CA, Levine JS, Zajonc DM, Rauch J. J Immunol 186 4771-4781 (2011)
  8. Lipid binding orientation within CD1d affects recognition of Borrelia burgorferi antigens by NKT cells. Wang J, Li Y, Kinjo Y, Mac TT, Gibson D, Painter GF, Kronenberg M, Zajonc DM. Proc Natl Acad Sci U S A 107 1535-1540 (2010)
  9. Natural lipid ligands associated with human CD1d targeted to different subcellular compartments. Yuan W, Kang SJ, Evans JE, Cresswell P. J Immunol 182 4784-4791 (2009)
  10. Conserved and heterogeneous lipid antigen specificities of CD1d-restricted NKT cell receptors. Brigl M, van den Elzen P, Chen X, Meyers JH, Wu D, Wong CH, Reddington F, Illarianov PA, Besra GS, Brenner MB, Gumperz JE. J Immunol 176 3625-3634 (2006)
  11. Crystal structures of mouse CD1d-iGb3 complex and its cognate Valpha14 T cell receptor suggest a model for dual recognition of foreign and self glycolipids. Zajonc DM, Savage PB, Bendelac A, Wilson IA, Teyton L. J Mol Biol 377 1104-1116 (2008)
  12. Invariant NKT cells limit activation of autoreactive CD1d-positive B cells. Wermeling F, Lind SM, Jordö ED, Cardell SL, Karlsson MC. J Exp Med 207 943-952 (2010)
  13. Endogenous phosphatidylcholine and a long spacer ligand stabilize the lipid-binding groove of CD1b. 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. EMBO J 25 3684-3692 (2006)
  14. MTP regulated by an alternate promoter is essential for NKT cell development. Dougan SK, Rava P, Hussain MM, Blumberg RS. J Exp Med 204 533-545 (2007)
  15. Role of lipid trimming and CD1 groove size in cellular antigen presentation. Cheng TY, Relloso M, Van Rhijn I, Young DC, Besra GS, Briken V, Zajonc DM, Wilson IA, Porcelli S, Moody DB. EMBO J 25 2989-2999 (2006)
  16. Structural reorganization of the antigen-binding groove of human CD1b for presentation of mycobacterial sulfoglycolipids. 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. Proc Natl Acad Sci U S A 108 17755-17760 (2011)
  17. Adaptability of the semi-invariant natural killer T-cell receptor towards structurally diverse CD1d-restricted ligands. Florence WC, Xia C, Gordy LE, Chen W, Zhang Y, Scott-Browne J, Kinjo Y, Yu KO, Keshipeddy S, Pellicci DG, Patel O, Kjer-Nielsen L, McCluskey J, Godfrey DI, Rossjohn J, Richardson SK, Porcelli SA, Howell AR, Hayakawa K, Gapin L, Zajonc DM, Wang PG, Joyce S. EMBO J 28 3579-3590 (2009)
  18. CD1c bypasses lysosomes to present a lipopeptide antigen with 12 amino acids. Van Rhijn I, Young DC, De Jong A, Vazquez J, Cheng TY, Talekar R, Barral DC, León L, Brenner MB, Katz JT, Riese R, Ruprecht RM, O'Connor PB, Costello CE, Porcelli SA, Briken V, Moody DB. J Exp Med 206 1409-1422 (2009)
  19. Crystal structure of human CD1e reveals a groove suited for lipid-exchange processes. 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. Proc Natl Acad Sci U S A 108 13230-13235 (2011)
  20. Identification of self-lipids presented by CD1c and CD1d proteins. Haig NA, Guan Z, Li D, McMichael A, Raetz CR, Xu XN. J Biol Chem 286 37692-37701 (2011)
  21. On/off TLR signaling decides proinflammatory or tolerogenic dendritic cell maturation upon CD1d-mediated interaction with invariant NKT cells. Caielli S, Conforti-Andreoni C, Di Pietro C, Usuelli V, Badami E, Malosio ML, Falcone M. J Immunol 185 7317-7329 (2010)
  22. Structural and mechanistic analyses of endo-glycoceramidase II, a membrane-associated family 5 glycosidase in the Apo and GM3 ganglioside-bound forms. Caines ME, Vaughan MD, Tarling CA, Hancock SM, Warren RA, Withers SG, Strynadka NC. J Biol Chem 282 14300-14308 (2007)
  23. NKT cells and IFN-gamma establish the regulatory environment for the control of diabetogenic T cells in the nonobese diabetic mouse. Cain JA, Smith JA, Ondr JK, Wang B, Katz JD. J Immunol 176 1645-1654 (2006)
  24. The crystal structure of avian CD1 reveals a smaller, more primordial antigen-binding pocket compared to mammalian CD1. Zajonc DM, Striegl H, Dascher CC, Wilson IA. Proc Natl Acad Sci U S A 105 17925-17930 (2008)
  25. Congenic analysis of the NKT cell control gene Nkt2 implicates the peroxisomal protein Pxmp4. Fletcher JM, Jordan MA, Snelgrove SL, Slattery RM, Dufour FD, Kyparissoudis K, Besra GS, Godfrey DI, Baxter AG. J Immunol 181 3400-3412 (2008)
  26. Alpha versus beta: are we on the way to resolve the mystery as to which is the endogenous ligand for natural killer T cells? Ilan Y. Clin Exp Immunol 158 300-307 (2009)
  27. Atypical sideways recognition of CD1a by autoreactive γδ T cell receptors. Wegrecki M, Ocampo TA, Gunasinghe SD, von Borstel A, Tin SY, Reijneveld JF, Cao TP, Gully BS, Le Nours J, Moody DB, Van Rhijn I, Rossjohn J. Nat Commun 13 3872 (2022)
  28. Importance of N-linked glycosylation in the functional expression of murine CD1d1. Sriram V, Willard CA, Liu J, Brutkiewicz RR. Immunology 123 272-281 (2008)
  29. Crystal structure of bovine CD1b3 with endogenously bound ligands. Girardi E, Wang J, Mac TT, Versluis C, Bhowruth V, Besra G, Heck AJ, Van Rhijn I, Zajonc DM. J Immunol 185 376-386 (2010)
  30. Linking inflammation to natural killer T cell activation. Salio M, Cerundolo V. PLoS Biol 7 e1000226 (2009)
  31. The structural and functional role of myelin fast-migrating cerebrosides: pathological importance in multiple sclerosis. Podbielska M, Levery SB, Hogan EL. Clin Lipidol 6 159-179 (2011)
  32. Liposomes of phosphatidylcholine and cholesterol induce an M2-like macrophage phenotype reprogrammable to M1 pattern with the involvement of B-1 cells. Cruz-Leal Y, Lucatelli Laurindo MF, Osugui L, Luzardo Mdel C, López-Requena A, Alonso ME, Álvarez C, Popi AF, Mariano M, Pérez R, Lanio ME. Immunobiology 219 403-415 (2014)
  33. Novel Adjuvant Based on the Pore-Forming Protein Sticholysin II Encapsulated into Liposomes Effectively Enhances the Antigen-Specific CTL-Mediated Immune Response. Laborde RJ, Sanchez-Ferras O, Luzardo MC, Cruz-Leal Y, Fernández A, Mesa C, Oliver L, Canet L, Abreu-Butin L, Nogueira CV, Tejuca M, Pazos F, Álvarez C, Alonso ME, Longo-Maugéri IM, Starnbach MN, Higgins DE, Fernández LE, Lanio ME. J Immunol 198 2772-2784 (2017)
  34. Design and Evaluation of ω-Hydroxy Fatty Acids Containing α-GalCer Analogues for CD1d-Mediated NKT Cell Activation. Lim C, Kim JH, Baek DJ, Lee JY, Cho M, Lee YS, Kang CY, Chung DH, Cho WJ, Kim S. ACS Med Chem Lett 5 331-335 (2014)
  35. Heteroaromatic Moieties in the Sphingosine Backbone of α-Galactosylceramides for Noncovalent Interactions with CD1d. Kim Y, Kim J, Oh K, Lee DS, Park SB. ACS Med Chem Lett 3 151-154 (2012)
  36. Self-glycerophospholipids activate murine phospholipid-reactive T cells and inhibit iNKT cell activation by competing with ligands for CD1d loading. Halder RC, Tran C, Prasad P, Wang J, Nallapothula D, Ishikawa T, Wang M, Zajonc DM, Singh RR. Eur J Immunol 49 242-254 (2019)
  37. Analysis of evolutionary conservation in CD1d molecules among primates. Saito N, Takahashi M, Akahata W, Ido E, Hidaka C, Ibuki K, Miura T, Hayami M, Takahashi H. Tissue Antigens 66 674-682 (2005)
  38. Molecular cloning, expression, and functional analysis of a predicted sulfotransferase STF9 from Mycobacterium avium. Hossain MM, Moriizumi Y, Tanaka S, Kimura M, Kakuta Y. Mol Cell Biochem 350 155-162 (2011)
  39. Synthesis of a 2"-deoxy-β-GalCer. Thakur MS, Khurana A, Kronenberg M, Howell AR. Molecules 19 10090-10102 (2014)
  40. Choline chloride attenuates the allergic airway disease by inhibiting the lysophosphatidylcholine induced response in mouse model. Bansal P, Singh N, Joshi J, Arora N, Gaur SN. Curr Res Pharmacol Drug Discov 3 100109 (2022)


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