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A molecular basis of human T cell receptor autoreactivity toward self-phospholipids.

Shahine A, Van Rhijn I, Cheng TY, Iwany S, Gras S, Moody DB, Rossjohn J
Sci Immunol 2 (2017)
Related entries: 5wjo, 5wke, 5wkg, 5wki

Cited: 29 times
EuropePMC logo PMID: 29054999

Abstract

Human T cell autoreactivity toward lipid antigens presented by CD1 proteins can manifest in numerous diseases, including psoriasis, contact hypersensitivities, and allergies. However, the molecular mechanisms for regulating T cell autoreactivity toward lipid antigens remain unclear. We determined the basis for T cell receptor (TCR) autoreactivity toward CD1b bound to self-phospholipids. The spectrum of self-antigens captured by CD1b skews toward abundant membrane phospholipids such as phosphatidylcholine and phosphatidylethanolamine. However, TCRs can specifically recognize rare phospholipids, including phosphatidylglycerol (PG). The structure of an autoreactive TCR bound to CD1b-PG shows that discrimination occurs through a marked induced fit movement of PG so that its polar head group fits snugly into the cationic cup of the TCR. Conversely, TCR binding toward ubiquitous self-phospholipids was sterically or electrostatically repelled. Accordingly, we describe a mechanism of TCR autoreactivity toward rare phospholipids and avoidance of autoreactivity to the most abundant self-phospholipids.

Reviews - 5wl1 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 - 5wl1 mentioned but not cited (3)

  1. A T-cell receptor escape channel allows broad T-cell response to CD1b and membrane phospholipids. 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. Nat Commun 10 56 (2019)
  2. A molecular basis of human T cell receptor autoreactivity toward self-phospholipids. Shahine A, Van Rhijn I, Cheng TY, Iwany S, Gras S, Moody DB, Rossjohn J. Sci Immunol 2 (2017)
  3. 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)


Reviews citing this publication (8)

  1. Lipids hide or step aside for CD1-autoreactive T cell receptors. Cotton RN, Shahine A, Rossjohn J, Moody DB. Curr Opin Immunol 52 93-99 (2018)
  2. The versatility of the CD1 lipid antigen presentation pathway. Chancellor A, Gadola SD, Mansour S. Immunology 154 196-203 (2018)
  3. 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)
  4. Membrane Lipid Composition: Effect on Membrane and Organelle Structure, Function and Compartmentalization and Therapeutic Avenues. Casares D, Escribá PV, Rosselló CA. Int J Mol Sci 20 (2019)
  5. The Conventional Nature of Non-MHC-Restricted T Cells. Lepore M, Mori L, De Libero G. Front Immunol 9 1365 (2018)
  6. CD1-mediated immune responses in mucosal tissues: molecular mechanisms underlying lipid antigen presentation system. Kim S, Cho S, Kim JH. Exp Mol Med 55 1858-1871 (2023)
  7. CD1: From Molecules to Diseases. Moody DB, Suliman S. F1000Res 6 1909 (2017)
  8. Phospholipid signaling in innate immune cells. O'Donnell VB, Rossjohn J, Wakelam MJ. J. Clin. Invest. 128 2670-2679 (2018)

Articles citing this publication (17)

  1. 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)
  2. T cell autoreactivity directed toward CD1c itself rather than toward carried self lipids. Wun KS, Reijneveld JF, Cheng TY, Ladell K, Uldrich AP, Le Nours J, Miners KL, McLaren JE, Grant EJ, Haigh OL, Watkins TS, Suliman S, Iwany S, Jimenez J, Calderon R, Tamara KL, Leon SR, Murray MB, Mayfield JA, Altman JD, Purcell AW, Miles JJ, Godfrey DI, Gras S, Price DA, Van Rhijn I, Moody DB, Rossjohn J. Nat. Immunol. 19 397-406 (2018)
  3. Detection of the Disorders of Glycerophospholipids and Amino Acids Metabolism in Lung Tissue From Male COPD Patients. Huang Q, Wu X, Gu Y, Wang T, Zhan Y, Chen J, Zeng Z, Lv Y, Zhao J, Xie J. Front Mol Biosci 9 839259 (2022)
  4. MHC Restriction: Where Are We Now? Zareie P, Farenc C, La Gruta NL. Viral Immunol 33 179-187 (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. Biochemical and Computational Assessment of Acute Phase Proteins in Dairy Cows Affected with Subclinical Mastitis. Ali A, Rehman MU, Mushtaq S, Ahmad SB, Khan A, Karan A, Bashir Wani A, Ganie SA, Mir MUR. Curr Issues Mol Biol 45 5317-5346 (2023)
  7. CD1 and MR1 recognition by human γδ T cells. Van Rhijn I, Le Nours J. Mol Immunol 133 95-100 (2021)
  8. 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)
  9. 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)
  10. Dynamic plasticity of the lipid antigen-binding site of CD1d is crucially favoured by acidic pH and helper proteins. Cuevas-Zuviría B, Mínguez-Toral M, Díaz-Perales A, Garrido-Arandia M, Pacios LF. Sci Rep 10 5714 (2020)
  11. How T cells grasp mycobacterial lipid antigens. Moody DB. Proc. Natl. Acad. Sci. U.S.A. 114 13312-13314 (2017)
  12. 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 (2021)
  13. 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)
  14. Maternal and Infant Immune Repertoire Sequencing Analysis Identifies Distinct Ig and TCR Development in Term and Preterm Infants. Le BL, Sper R, Nielsen SCA, Pineda S, Nguyen QH, Lee JY, Boyd SD, MacKenzie TC, Sirota M. J Immunol 207 2445-2455 (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. T Cell Receptor Repertoire Analysis Reveals Signatures of T Cell Responses to Human Mycobacterium tuberculosis. Shao MM, Yi FS, Huang ZY, Peng P, Wu FY, Shi HZ, Zhai K. Front Microbiol 13 829694 (2022)
  17. 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)


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