Core fucosylation of the T cell receptor is required for T cell activation

Frontiers in Immunology

Volumn 9, Issue JAN, 2018, Pages

  Liang, Wei ^a   Mao, Shanshan ^a   Sun, Shijie ^a   Li, Ming ^a   Li, Zhi ^b   Yu, Rui ^a   Ma, Tonghui ^a   Gu, Jianguo ^c   Zhang, Jianing ^d   Taniguchi, Naoyuki ^e   Li, Wenzhe ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b Dalian Municipal Central Hospital   (China)

^c TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^d DALIAN UNIVERSITY OF TECHNOLOGY   (China)

^e RIKEN   (Japan)

Author keywords

Core fucosylation; Systemic lupus erythematosus; T cell activation; T cell receptor; T B cell interaction

Indexed keywords

ALPHA LEVO FUCOSIDASE; CHEMOKINE RECEPTOR CXCR4; FUCOSYLTRANSFERASE; GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LECTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR;

ADULT; AGED; ALLERGIC ENCEPHALOMYELITIS; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL LYSATE; CELL PROLIFERATION; CELL SELECTION; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; FUCOSYLATION; HUMAN; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOPRECIPITATION; MALE; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

EID: 85041207339     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.00078     Document Type: Article

References (47)

1. Yin Y, Choi SC, Xu Z, Perry DJ, Seay H, Croker BP, et al. Normalization of CD4+ T cell metabolism reverses lupus. Sci Transl Med (2015) 7(274):274ra18. doi:10.1126/scitranslmed.aaa0835
2. Rupanagudi KV, Kulkarni OP, Lichtnekert J, Darisipudi MN, Mulay SR, Schott B, et al. Cathepsin S inhibition suppresses systemic lupus erythematosus and lupus nephritis because cathepsin S is essential for MHC class II-mediated CD4 T cell and B cell priming. Ann Rheum Dis (2015) 74(2):452-63. doi:10.1136/annrheumdis-2013-203717
3. Reinherz EL, Tan K, Tang L, Kern P, Liu J, Xiong Y, et al. The crystal structure of a T cell receptor in complex with peptide and MHC class II. Science (1999) 286(5446):1913-21. doi:10.1126/science.286.5446.1913
4. Lee KH, Holdorf AD, Dustin ML, Chan AC, Allen PM, Shaw AS. T cell receptor signaling precedes immunological synapse formation. Science (2002) 295(5559):1539-42. doi:10.1126/science.1067710
5. Johnson JL, Jones MB, Ryan SO, Cobb BA. The regulatory power of glycans and their binding partners in immunity. Trends Immunol (2013) 34(6):290-8. doi:10.1016/j.it.2013.01.006
6. Rudd PM, Wormald MR, Stanfield RL, Huang M, Mattsson N, Speir JA, et al. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J Mol Biol (1999) 293(2):351-66. doi:10.1006/jmbi.1999.3104
7. Daniels MA, Hogquist KA, Jameson SC. Sweet 'n' sour: the impact of differential glycosylation on T cell responses. Nat Immunol (2002) 3(10):903-10. doi:10.1038/ni1002-903
8. Lowe JB. Glycosylation, immunity, and autoimmunity. Cell (2001) 104(6):809-12. doi:10.1016/S0092-8674(01)00277-X
9. Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA. Glycosylation and the immune system. Science (2001) 291(5512):2370-6. doi:10.1126/science.291.5512.2370
10. Okada M, Chikuma S, Kondo T, Hibino S, Machiyama H, Yokosuka T, et al. Blockage of core fucosylation reduces cell-surface expression of PD-1 and promotes anti-tumor immune responses of T cells. Cell Rep (2017) 20(5):1017-28. doi:10.1016/j.celrep.2017.07.027
11. Demetriou M, Granovsky M, Quaggin S, Dennis JW. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature (2001) 409(6821):733-9. doi:10.1038/35055582
12. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, et al. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell (2007) 129(1):123-34. doi:10.1016/j.cell.2007.01.049
13. Starr TK, Daniels MA, Lucido MM, Jameson SC, Hogquist KA. Thymocyte sensitivity and supramolecular activation cluster formation are developmentally regulated: a partial role for sialylation. J Immunol (2003) 171(9):4512-20. doi:10.4049/jimmunol.171.9.4512
14. Moore GT, Brown SJ, Winterhalter AC, Lust M, Salvaris EJ, Selan C, et al. Glycosylation changes in hFUT1 transgenic mice increase TCR signaling and apoptosis resulting in thymocyte maturation arrest. Mol Immunol (2008) 45(8):2401-10. doi:10.1016/j.molimm.2007.11.006
15. Kuball J, Hauptrock B, Malina V, Antunes E, Voss RH, WolflM, et al. Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J Exp Med (2009) 206(2):463-75. doi:10.1084/jem.20082487
16. Calderon AD, Liu Y, Li X, Wang X, Chen X, Li L, et al. Substrate specificity of FUT8 and chemoenzymatic synthesis of core-fucosylated asymmetric N-glycans. Org Biomol Chem (2016) 14(17):4027-31. doi:10.1039/c6ob00586a
17. Garcia KC, Degano M, Stanfield RL, Brunmark A, Jackson MR, Peterson PA, et al. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science (1996) 274(5285):209-19. doi:10.1126/science.274.5285.209
18. Batista FD, Harwood NE. The who, how and where of antigen presentation to B cells. Nat Rev Immunol (2009) 9(1):15-27. doi:10.1038/nri2454
19. Wang X, Inoue S, Gu J, Miyoshi E, Noda K, Li W, et al. Dysregulation of TGF-beta1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc Natl Acad Sci U S A (2005) 102(44):15791-6. doi:10.1073/pnas.0507375102
20. Uozumi N, Teshima T, Yamamoto T, Nishikawa A, Gao YE, Miyoshi E, et al. A fluorescent assay method for GDP-L-Fuc:N-acetyl-beta-D-glucosaminide alpha 1-6fucosyltransferase activity, involving high performance liquid chromatography. J Biochem (1996) 120(2):385-92. doi:10.1093/oxfordjournals.jbchem.a021424
21. Watson AR, Lee WT. Differences in signaling molecule organization between naive and memory CD4+ T lymphocytes. J Immunol (2004) 173(1):33-41. doi:10.4049/jimmunol.173.1.33
22. Tateno H, Nakamura-Tsuruta S, Hirabayashi J. Comparative analysis of core-fucose-binding lectins from Lens culinaris and Pisum sativum using frontal affinity chromatography. Glycobiology (2009) 19(5):527-36. doi:10.1093/glycob/cwp016
23. Mao L, Hou H, Wu S, Zhou Y, Wang J, Yu J, et al. TIGIT signalling pathway negatively regulates CD4+ T-cell responses in systemic lupus erythematosus. Immunology (2017) 151(3):280-90. doi:10.1111/imm.12715
24. Scott CA, Peterson PA, Teyton L, Wilson IA. Crystal structures of two I-Ad-peptide complexes reveal that high affinity can be achieved without large anchor residues. Immunity (1998) 8(3):319-29. doi:10.1016/S1074-7613(00)80537-3
25. O'Flaherty R, Harbison AM, Hanley PJ, Taron CH, Fadda E, Rudd PM. Aminoquinoline fluorescent labels obstruct efficient removal of N-glycan core alpha(1-6) fucose by bovine kidney alpha-l-fucosidase (BKF). J Proteome Res (2017) 16(11):4237-43. doi:10.1021/acs.jproteome.7b00580
26. Parekh RB, Roitt IM, Isenberg DA, Dwek RA, Ansell BM, Rademacher TW. Galactosylation of IgG associated oligosaccharides: reduction in patients with adult and juvenile onset rheumatoid arthritis and relation to disease activity. Lancet (1988) 1(8592):966-9. doi:10.1016/S0140-6736(88)91781-3
27. Ercan A, Cui J, Chatterton DE, Deane KD, Hazen MM, Brintnell W, et al. Aberrant IgG galactosylation precedes disease onset, correlates with disease activity, and is prevalent in autoantibodies in rheumatoid arthritis. Arthritis Rheum (2010) 62(8):2239-48. doi:10.1002/art.27533
28. Matsumoto A, Shikata K, Takeuchi F, Kojima N, Mizuochi T. Autoantibody activity of IgG rheumatoid factor increases with decreasing levels of galactosylation and sialylation. J Biochem (2000) 128(4):621-8. doi:10.1093/oxfordjournals.jbchem.a022794
29. Espy C, Morelle W, Kavian N, Grange P, Goulvestre C, Viallon V, et al. Sialylation levels of anti-proteinase 3 antibodies are associated with the activity of granulomatosis with polyangiitis (Wegener's). Arthritis Rheum (2011) 63(7):2105-15. doi:10.1002/art.30362
30. Ramos-Martinez E, Lascurain R, Tenorio EP, Sanchez-Gonzalez A, Chavez-Rueda K, Chavez-Sanchez L, et al. Differential expression of O-glycans in CD4(+) T lymphocytes from patients with systemic lupus erythematosus. Tohoku J Exp Med (2016) 240(1):79-89. doi:10.1620/tjem.240.79
31. Vuckovic F, Kristic J, Gudelj I, Teruel M, Keser T, Pezer M, et al. Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome. Arthritis Rheumatol (2015) 67(11):2978-89. doi:10.1002/art.39273
32. Fujii H, Shinzaki S, Iijima H, Wakamatsu K, Iwamoto C, Sobajima T, et al. Core fucosylation on T cells, required for activation of T-cell receptor signaling and induction of colitis in mice, is increased in patients with inflammatory bowel disease. Gastroenterology (2016) 150(7):1620-32. doi:10.1053/j.gastro.2016.03.002
33. Alarcon B, Gil D, Delgado P, Schamel WW. Initiation of TCR signaling: regulation within CD3 dimers. Immunol Rev (2003) 191:38-46. doi:10.1034/j.1600-065X.2003.00017.x
34. Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today (1998) 19(9):395-404. doi:10.1016/S0167-5699(98)01299-7
35. Kass I, Buckle AM, Borg NA. Understanding the structural dynamics of TCR-pMHC complex interactions. Trends Immunol (2014) 35(12):604-12. doi:10.1016/j.it.2014.10.005
36. Alam SM, Davies GM, Lin CM, Zal T, Nasholds W, Jameson SC, et al. Qualitative and quantitative differences in T cell receptor binding of agonist and antagonist ligands. Immunity (1999) 10(2):227-37. doi:10.1016/S1074-7613(00)80023-0
37. Schamel WW, Arechaga I, Risueno RM, van Santen HM, Cabezas P, Risco C, et al. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J Exp Med (2005) 202(4):493-503. doi:10.1084/jem.20042155
38. Stubbs HJ, Lih JJ, Gustafson TL, Rice KG. Influence of core fucosylation on the flexibility of a biantennary N-linked oligosaccharide. Biochemistry (1996) 35(3):937-47. doi:10.1021/bi9513719
39. Wormald MR, Dwek RA. Glycoproteins: glycan presentation and protein-fold stability. Structure (1999) 7(7):R155-60. doi:10.1016/S0969-2126(99)80095-1
40. Wolfert MA, Boons GJ. Adaptive immune activation: glycosylation does matter. Nat Chem Biol (2013) 9(12):776-84. doi:10.1038/nchembio.1403
41. Lehrman MA, Hill RL. The binding of fucose-containing glycoproteins by hepatic lectins. Purification of a fucose-binding lectin from rat liver. J Biol Chem (1986) 261(16):7419-25
42. Moulton VR, Tsokos GC. T cell signaling abnormalities contribute to aberrant immune cell function and autoimmunity. J Clin Invest (2015) 125(6):2220-7. doi:10.1172/jci78087
43. Mi XB, Zeng FQ. Hypomethylation of interleukin-4 and-6 promoters in T cells from systemic lupus erythematosus patients. Acta Pharmacol Sin (2008) 29(1):105-12. doi:10.1111/j.1745-7254.2008.00739.x
44. Gerez L, Shkolnik T, Hirschmann O, Lorber M, Arad G, Kaempfer R. Hyperinducible expression of the interferon-gamma (IFN-gamma) gene and its suppression in systemic lupus erythematosus (SLE). Clin Exp Immunol (1997) 109(2):296-303. doi:10.1046/j.1365-2249.1997.4471345.x
45. Linker-Israeli M, Deans RJ, Wallace DJ, Prehn J, Ozeri-Chen T, Klinenberg JR. Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J Immunol (1991) 147(1):117-23
46. Grondal G, Gunnarsson I, Ronnelid J, Rogberg S, Klareskog L, Lundberg I. Cytokine production, serum levels and disease activity in systemic lupus erythematosus. Clin Exp Rheumatol (2000) 18(5):565-70
47. Grigorian A, Lee SU, Tian W, Chen IJ, Gao G, Mendelsohn R, et al. Control of T cell-mediated autoimmunity by metabolite flux to N-glycan biosynthesis. J Biol Chem (2007) 282(27):20027-35. doi:10.1074/jbc. M701890200