Mycobacterial Phosphatidylinositol Mannoside is a Natural Antigen for CD1d-restricted T Cells

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Jul 10

PMID 15243159

Citations 133

Authors

Karsten Fischer

Emmanuel Scotet

Marcus Niemeyer

Heidrun Koebernick

Jens Zerrahn

Sophie Maillet

Robert Hurwitz

Mischo Kursar

Marc Bonneville

Stefan H E Kaufmann

Ulrich E Schaible

Affiliations

Soon will be listed here.

Abstract

A group of T cells recognizes glycolipids presented by molecules of the CD1 family. The CD1d-restricted natural killer T cells (NKT cells) are primarily considered to be self-reactive. By employing CD1d-binding and T cell assays, the following structural parameters for presentation by CD1d were defined for a number of mycobacterial and mammalian lipids: two acyl chains facilitated binding, and a polar head group was essential for T cell recognition. Of the mycobacterial lipids tested, only a phosphatidylinositol mannoside (PIM) fulfilled the requirements for CD1d binding and NKT cell stimulation. This PIM activated human and murine NKT cells via CD1d, thereby triggering antigen-specific IFN-gamma production and cell-mediated cytotoxicity, and PIM-loaded CD1d tetramers identified a subpopulation of murine and human NKT cells. This phospholipid, therefore, represents a mycobacterial antigen recognized by T cells in the context of CD1d.

Citing Articles

Intestinal mucosal immunity and type 1 diabetes: Non-negligible communication between gut and pancreas.

Liu R, Zhang J, Chen S, Xiao Y, Hu J, Zhou Z Diabetes Obes Metab. 2024; 27(3):1045-1064.

PMID: 39618164 PMC: 11802406. DOI: 10.1111/dom.16101.

Impaired endocytosis and accumulation in early endosomal compartments defines herpes simplex virus-mediated disruption of the nonclassical MHC class I-related molecule MR1.

Samer C, McWilliam H, McSharry B, Burchfield J, Stanton R, Rossjohn J J Biol Chem. 2024; 300(10):107748.

PMID: 39260697 PMC: 11736056. DOI: 10.1016/j.jbc.2024.107748.

A structural perspective of how T cell receptors recognize the CD1 family of lipid antigen-presenting molecules.

Cao T, Shahine A, Cox L, Besra G, Moody D, Rossjohn J J Biol Chem. 2024; 300(8):107511.

PMID: 38945451 PMC: 11780374. DOI: 10.1016/j.jbc.2024.107511.

CD1-mediated immune responses in mucosal tissues: molecular mechanisms underlying lipid antigen presentation system.

Kim S, Cho S, Kim J Exp Mol Med. 2023; 55(9):1858-1871.

PMID: 37696897 PMC: 10545705. DOI: 10.1038/s12276-023-01053-6.

Invariant natural killer T cells in lung diseases.

Jeong D, Woo Y, Chung D Exp Mol Med. 2023; 55(9):1885-1894.

PMID: 37696892 PMC: 10545712. DOI: 10.1038/s12276-023-01024-x.

References

Szalay G, Zugel U, Ladel C, Kaufmann S . Participation of group 2 CD1 molecules in the control of murine tuberculosis. Microbes Infect. 1999; 1(14):1153-7. DOI: 10.1016/s1286-4579(99)00248-8. View

Naidenko O, Maher J, Ernst W, Sakai T, Modlin R, Kronenberg M . Binding and antigen presentation of ceramide-containing glycolipids by soluble mouse and human CD1d molecules. J Exp Med. 1999; 190(8):1069-80. PMC: 2195664. DOI: 10.1084/jem.190.8.1069. View

Schaible U, Hagens K, Fischer K, Collins H, Kaufmann S . Intersection of group I CD1 molecules and mycobacteria in different intracellular compartments of dendritic cells. J Immunol. 2000; 164(9):4843-52. DOI: 10.4049/jimmunol.164.9.4843. View

Molano A, Park S, Chiu Y, Nosseir S, Bendelac A, Tsuji M . Cutting edge: the IgG response to the circumsporozoite protein is MHC class II-dependent and CD1d-independent: exploring the role of GPIs in NK T cell activation and antimalarial responses. J Immunol. 2000; 164(10):5005-9. DOI: 10.4049/jimmunol.164.10.5005. View

Matsuda J, Naidenko O, Gapin L, Nakayama T, Taniguchi M, Wang C . Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J Exp Med. 2000; 192(5):741-54. PMC: 2193268. DOI: 10.1084/jem.192.5.741. View

Schaible U, Kaufmann S . CD1 and CD1-restricted T cells in infections with intracellular bacteria. Trends Microbiol. 2000; 8(9):419-25. DOI: 10.1016/s0966-842x(00)01829-1. View

Watts C . Antigen processing in the endocytic compartment. Curr Opin Immunol. 2001; 13(1):26-31. DOI: 10.1016/s0952-7915(00)00177-1. View

Matsuda J, Kronenberg M . Presentation of self and microbial lipids by CD1 molecules. Curr Opin Immunol. 2001; 13(1):19-25. DOI: 10.1016/s0952-7915(00)00176-x. View

Prigozy T, Naidenko O, Qasba P, Elewaut D, Brossay L, Khurana A . Glycolipid antigen processing for presentation by CD1d molecules. Science. 2001; 291(5504):664-7. DOI: 10.1126/science.291.5504.664. View

10.

Park S, Weiss A, Benlagha K, Kyin T, Teyton L, Bendelac A . The mouse CD1d-restricted repertoire is dominated by a few autoreactive T cell receptor families. J Exp Med. 2001; 193(8):893-904. PMC: 2193401. DOI: 10.1084/jem.193.8.893. View

11.

Wang B, Geng Y, Wang C . CD1-restricted NK T cells protect nonobese diabetic mice from developing diabetes. J Exp Med. 2001; 194(3):313-20. PMC: 2193465. DOI: 10.1084/jem.194.3.313. View

12.

Fischer K, Chatterjee D, Torrelles J, Brennan P, Kaufmann S, Schaible U . Mycobacterial lysocardiolipin is exported from phagosomes upon cleavage of cardiolipin by a macrophage-derived lysosomal phospholipase A2. J Immunol. 2001; 167(4):2187-92. DOI: 10.4049/jimmunol.167.4.2187. View

13.

Gilleron M, Ronet C, Mempel M, Monsarrat B, Gachelin G, Puzo G . Acylation state of the phosphatidylinositol mannosides from Mycobacterium bovis bacillus Calmette Guérin and ability to induce granuloma and recruit natural killer T cells. J Biol Chem. 2001; 276(37):34896-904. DOI: 10.1074/jbc.M103908200. View

14.

Miyamoto K, Miyake S, Yamamura T . A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature. 2001; 413(6855):531-4. DOI: 10.1038/35097097. View

15.

Mittrucker H, Kursar M, Kohler A, HURWITZ R, Kaufmann S . Role of CD28 for the generation and expansion of antigen-specific CD8(+) T lymphocytes during infection with Listeria monocytogenes. J Immunol. 2001; 167(10):5620-7. DOI: 10.4049/jimmunol.167.10.5620. View

16.

Mempel M, Ronet C, Suarez F, Gilleron M, Puzo G, Van Kaer L . Natural killer T cells restricted by the monomorphic MHC class 1b CD1d1 molecules behave like inflammatory cells. J Immunol. 2001; 168(1):365-71. DOI: 10.4049/jimmunol.168.1.365. View

17.

Fischer K, Collins H, Taniguchi M, Kaufmann S, Schaible U . IL-4 and T cells are required for the generation of IgG1 isotype antibodies against cardiolipin. J Immunol. 2002; 168(6):2689-94. DOI: 10.4049/jimmunol.168.6.2689. View

18.

Kursar M, Bonhagen K, Kohler A, Kamradt T, Kaufmann S, Mittrucker H . Organ-specific CD4+ T cell response during Listeria monocytogenes infection. J Immunol. 2002; 168(12):6382-7. DOI: 10.4049/jimmunol.168.12.6382. View

19.

Procopio D, Almeida I, Torrecilhas A, Cardoso J, Teyton L, Travassos L . Glycosylphosphatidylinositol-anchored mucin-like glycoproteins from Trypanosoma cruzi bind to CD1d but do not elicit dominant innate or adaptive immune responses via the CD1d/NKT cell pathway. J Immunol. 2002; 169(7):3926-33. DOI: 10.4049/jimmunol.169.7.3926. View

20.

Sugawara I, Yamada H, Mizuno S, Li C, Nakayama T, Taniguchi M . Mycobacterial infection in natural killer T cell knockout mice. Tuberculosis (Edinb). 2002; 82(2-3):97-104. DOI: 10.1054/tube.2002.0331. View