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A T-cell receptor escape channel allows broad T-cell response to CD1b and membrane phospholipids.

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Shahine A, Reinink P, Reijneveld JF, Gras S, Holzheimer M, Cheng TY, Minnaard AJ, Altman JD, Lenz S, Prandi J, Kubler-Kielb J, Moody DB, Rossjohn J, Van Rhijn I
OpenAccess logo Nat Commun 10 56 (2019)
Related entries: 6cuh, 6d64

Cited: 23 times
EuropePMC logo PMID: 30610190

Abstract

CD1 proteins are expressed on dendritic cells, where they display lipid antigens to T-cell receptors (TCRs). Here we describe T-cell autoreactivity towards ubiquitous human membrane phospholipids presented by CD1b. These T-cells discriminate between two major types of lipids, sphingolipids and phospholipids, but were broadly cross-reactive towards diverse phospholipids including phosphatidylcholine, phosphatidylinositol and phosphatidylethanolamine. The crystal structure of a representative TCR bound to CD1b-phosphatidylcholine provides a molecular mechanism for this promiscuous recognition. We observe a lateral escape channel in the TCR, which shunted phospholipid head groups sideways along the CD1b-TCR interface, without contacting the TCR. Instead the TCR recognition site involved the neck region phosphate that is common to all major self-phospholipids but absent in sphingolipids. Whereas prior studies have focused on foreign lipids or rare self-lipids, we define a new molecular mechanism of promiscuous recognition of common self-phospholipids including those that are known targets in human autoimmune disease.

Reviews - 6cug mentioned but not cited (1)

  1. Novel Molecular Insights into Human Lipid-Mediated T Cell Immunity. Shahine A, Wegrecki M, Le Nours J. Int J Mol Sci 22 2617 (2021)

Articles - 6cug mentioned but not cited (3)

  1. Structural basis of T cell receptor specificity and cross-reactivity of two HLA-DQ2.5-restricted gluten epitopes in celiac disease. Ciacchi L, Farenc C, Dahal-Koirala S, Petersen J, Sollid LM, Reid HH, Rossjohn J. J Biol Chem 298 101619 (2022)
  2. A Direct Role for the CD1b Endogenous Spacer in the Recognition of a Mycobacterium tuberculosis Antigen by T-Cell Receptors. Camacho F, Moreno E, Garcia-Alles LF, Chinea Santiago G, Gilleron M, Vasquez A, Choong YS, Reyes F, Norazmi MN, Sarmiento ME, Acosta A. Front Immunol 11 566710 (2020)
  3. αβ T-cell receptor recognition of self-phosphatidylinositol presented by CD1b. Farquhar R, Van Rhijn I, Moody DB, Rossjohn J, Shahine A. J Biol Chem 299 102849 (2023)


Reviews citing this publication (3)

  1. Fat of the Gut: Epithelial Phospholipids in Inflammatory Bowel Diseases. Boldyreva LV, Morozova MV, Saydakova SS, Kozhevnikova EN. Int J Mol Sci 22 11682 (2021)
  2. CD1 displays its own negative regulators. Shahine A, Van Rhijn I, Rossjohn J, Moody DB. Curr Opin Immunol 83 102339 (2023)
  3. Immunogenic molecules associated with gut bacterial cell walls: chemical structures, immune-modulating functions, and mechanisms. Yin R, Wang T, Dai H, Han J, Sun J, Liu N, Dong W, Zhong J, Liu H. Protein Cell 14 776-785 (2023)

Articles citing this publication (16)

  1. Human γδ T cells recognize CD1b by two distinct mechanisms. Reijneveld JF, Ocampo TA, Shahine A, Gully BS, Vantourout P, Hayday AC, Rossjohn J, Moody DB, Van Rhijn I. Proc Natl Acad Sci U S A 117 22944-22952 (2020)
  2. Human skin is colonized by T cells that recognize CD1a independently of lipid. Cotton RN, Cheng TY, Wegrecki M, Le Nours J, Orgill DP, Pomahac B, Talbot SG, Willis RA, Altman JD, de Jong A, Ogg G, Van Rhijn I, Rossjohn J, Clark RA, Moody DB. J Clin Invest 131 140706 (2021)
  3. Transcriptomic Analyses Revealed Systemic Alterations in Gene Expression in Circulation and Tumor Microenvironment of Colorectal Cancer Patients. Shaath H, Toor SM, Nair VS, Elkord E, Alajez NM. Cancers (Basel) 11 E1994 (2019)
  4. CD1b Tetramers Broadly Detect T Cells That Correlate With Mycobacterial Exposure but Not Tuberculosis Disease State. Lopez K, Iwany SK, Suliman S, Reijneveld JF, Ocampo TA, Jimenez J, Calderon R, Lecca L, Murray MB, Moody DB, Van Rhijn I. Front Immunol 11 199 (2020)
  5. Staphylococcal phosphatidylglycerol antigens activate human T cells via CD1a. Monnot GC, Wegrecki M, Cheng TY, Chen YL, Sallee BN, Chakravarthy R, Karantza IM, Tin SY, Khaleel AE, Monga I, Uwakwe LN, Tillman A, Cheng B, Youssef S, Ng SW, Shahine A, Garcia-Vilas JA, Uhlemann AC, Bordone LA, Han A, Rohde CH, Ogg G, Moody DB, Rossjohn J, de Jong A. Nat Immunol 24 110-122 (2023)
  6. A TCR β-Chain Motif Biases toward Recognition of Human CD1 Proteins. Reinink P, Shahine A, Gras S, Cheng TY, Farquhar R, Lopez K, Suliman SA, Reijneveld JF, Le Nours J, Tan LL, León SR, Jimenez J, Calderon R, Lecca L, Murray MB, Rossjohn J, Moody DB, Van Rhijn I. J Immunol 203 3395-3406 (2019)
  7. CD1b presents self and Borrelia burgdorferi diacylglycerols to human T cells. Reinink P, Souter MNT, Cheng TY, van Gorkom T, Lenz S, Kubler-Kielb J, Strle K, Kremer K, Thijsen SFT, Steere AC, Godfrey DI, Pellicci DG, Moody DB, Van Rhijn I. Eur J Immunol 49 737-746 (2019)
  8. CD36 family members are TCR-independent ligands for CD1 antigen-presenting molecules. Gherardin NA, Redmond SJ, McWilliam HEG, Almeida CF, Gourley KHA, Seneviratna R, Li S, De Rose R, Ross FJ, Nguyen-Robertson CV, Su S, Ritchie ME, Villadangos JA, Moody DB, Pellicci DG, Uldrich AP, Godfrey DI. Sci Immunol 6 eabg4176 (2021)
  9. MHC Restriction: Where Are We Now? Zareie P, Farenc C, La Gruta NL. Viral Immunol 33 179-187 (2020)
  10. Synthetic mycobacterial diacyl trehaloses reveal differential recognition by human T cell receptors and the C-type lectin Mincle. Reijneveld JF, Holzheimer M, Young DC, Lopez K, Suliman S, Jimenez J, Calderon R, Lecca L, Murray MB, Ishikawa E, Yamasaki S, Minnaard AJ, Moody DB, Van Rhijn I. Sci Rep 11 2010 (2021)
  11. CD1 lipidomes reveal lipid-binding motifs and size-based antigen-display mechanisms. Huang S, Shahine A, Cheng TY, Chen YL, Ng SW, Balaji GR, Farquhar R, Gras S, Hardman CS, Altman JD, Tahiri N, Minnaard AJ, Ogg GS, Mayfield JA, Rossjohn J, Moody DB. Cell 186 4583-4596.e13 (2023)
  12. CD1B is a Potential Prognostic Biomarker Associated with Tumor Mutation Burden and Promotes Antitumor Immunity in Lung Adenocarcinoma. Li Z, Feng Y, Li P, Wang S, Liu X, Xia S. Int J Gen Med 15 3809-3826 (2022)
  13. Structural Dynamics of the Lipid Antigen-Binding Site of CD1d Protein. Cuevas-Zuviría B, Mínguez-Toral M, Díaz-Perales A, Garrido-Arandia M, Pacios LF. Biomolecules 10 E532 (2020)
  14. Role of Group 1 CD1-Restricted T Cells in Host Defense and Inflammatory Diseases. Morgun E, Cao L, Wang CR. Crit Rev Immunol 41 1-21 (2021)
  15. Rational design of a hydrolysis-resistant mycobacterial phosphoglycolipid antigen presented by CD1c to T cells. Reijneveld JF, Marino L, Cao TP, Cheng TY, Dam D, Shahine A, Witte MD, Filippov DV, Suliman S, van der Marel GA, Moody DB, Minnaard AJ, Rossjohn J, Codée JDC, Van Rhijn I. J Biol Chem 297 101197 (2021)
  16. Liposomes have a direct effect on multiple myeloma: a Mendelian randomization study. Zhong Y, Li Y, Sun W, Xiao M. Front Oncol 14 1404744 (2024)


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