Differential expression of O-Glycans in CD4+ T lymphocytes from patients with systemic lupus erythematosus

Tohoku Journal of Experimental Medicine

Volumn 240, Issue 1, 2016, Pages 79-89

  Ramos Martínez, Edgar ^a   Lascurain, Ricardo ^b,c   Tenorio, Eda Patricia ^b   Sánchez González, Antonio ^d   Chávez Rueda, Karina ^a   Chávez Sánchez, Luis ^a   Jara Quezada, Luis J ^d   Chávez Sánchez, Raúl ^b   Zenteno, Edgar ^b   Blanco Favela, Francisco ^a  

^a HOSPITAL DE PEDIATRÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c INSTITUTO NACIONAL DE ENFERMEDADES RESPIRATORIAS   (Mexico)

^d HOSPITAL DE ESPECIALIDADES   (Mexico)

Author keywords

Lectin; O glycosylation; SLEDAI; Systemic lupus erythematosus; T cells

Indexed keywords

AMARANTHUS LEUCOCARPUS LECTIN; DISACCHARIDE; GLYCAN; JACALIN; LECTIN; MAAKIA AMURENSIS AGGLUTININ; MUCIN TYPE O GLYCAN; PEANUT AGGLUTININ; SAMBUCUS NIGRA AGGLUTININ; SIALIC ACID; UNCLASSIFIED DRUG; GLYCOPROTEIN; LIGAND; N ACETYLNEURAMINIC ACID; PLANT LECTIN; POLYSACCHARIDE;

ADULT; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL ISOLATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; FEMALE; FLOW CYTOMETRY; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SLEDAI; SYSTEMIC LUPUS ERYTHEMATOSUS; BLOOD; GLYCOSYLATION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; METABOLISM;

ADULT; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; LIGANDS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; N-ACETYLNEURAMINIC ACID; PLANT LECTINS; POLYSACCHARIDES; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84987725343     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tjem.240.79     Document Type: Article

References (47)

1. Anand, A., Dean, G.S., Quereshi, K., Isenberg, D.A. & Lydyard, P.M. (2002) Characterization of CD3+ CD4-CD8-(double negative) T cells in patients with systemic lupus erythematosus: activation markers. Lupus, 11, 493-500
2. Antonopoulos, A., Demotte, N., Stroobant, V., Haslam, S.M., van der Bruggen, P. & Dell, A. (2012) Loss of effector function of human cytolytic T lymphocytes is accompanied by major alterations in N-and O-glycosylation. J. Biol. Chem., 287, 11240-11251
3. Bagwell, C.B. (1996) A journey through flow cytometric immunofluoresence analyses: Finding accurate and robust algorithms that estimate positive fraction distributions. Clin. Immunol. Newsletter, 16, 33-37
4. Blanco, F., Kalsi, J. & Isenberg, D.A. (1991) Analysis of antibodies to RNA in patients with systemic lupus erythematosus and other autoimmune rheumatic diseases. Clin. Exp. Immunol., 86, 66-70
5. Blanco, F., Kalsi, J., Ravirajan, C.T., Speight, P., Bradwell, A.R. & Isenberg, D.A. (1992) IgG subclasses in systemic lupus erythematosus and other autoimmune rheumatic diseases. Lupus, 1, 391-399
6. Bombardier, C., Gladman, D.D., Urowitz, M.B., Caron, D. & Chang, D.H. (1992) Committee on Prognosis Studies in SLE Derivation of the SLEDAI: a disease activity index for lupus patients. Arthritis Rheum., 35, 630-640
7. Brockhausen, I., Schachter, H. & Stanley, P. (2009) O-GalNAc Glycans. In Essentials of Glycobiology, 2nd ed., edited by Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R., Hart, G.W. & Etzler, M.E. Cold Spring Harbor Laboratory Press, New York, pp. 115-126
8. Clark, M.C. & Baum, L.G. (2012) T cells modulate glycans on CD43 and CD45 during development and activation, signal regulation, and survival. Ann. NY Acad. Sci., 1253, 58-67
9. Cozzani, E., Drosera, M., Gasparini, G. & Parodi, A. (2014) Serology of lupus erythematosus: correlation between immunopathological features and clinical aspects. Autoimmun. Dis., 2014, 321359
10. Crispín, J.C., Oukka, M., Bayliss, G., Cohen, R.A., Van Beek, C.A., Stillman, I.E., Kyttaris, V.C., Juang, Y.T. & Tsokos, G.C. (2008) Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol., 181, 8761-8766
11. Crispín, J.C. & Tsokos, G.C. (2009) Human TCR-alpha beta+ CD4-CD8-T cells can derive from CD8+ T cells and display an inflammatory effector phenotype. J. Immunol., 183, 4675-4681
12. Daniels, M.A., Hogquist, K.A. & Jameson, S.C. (2002) Sweat ʻs’ sour: the impact of differential glycosylation on T cell responses. Nat. Immunol., 3, 903-910
13. Dhir, V., Singh, A.P., Aggarwal, A., Naik, S. & Misra, R. (2009) Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T-cell frequency: a cross-sectional and longitudinal study. Lupus, 18, 785-791
14. Dumont, F. & Habbersett, R.G. (1982) Unusual cell surface properties of the T lymphocyte population expanding in MRL/ Mp-lpr/lpr mice. Immunol., 47, 271-281
15. Fortune, F. & Lehner, T. (1988) Phenotypic expression of Vicia villosa binding T cell subsets, as markers of contrasuppressor cells in systemic lupus erythematosus. Clin. Exp. Immunol., 74, 100-104
16. Fortune, F., Walker, J., Lefrancois, M. & Lehner, T. (1994) The expression of carbohydrate antigens in activated T cells and in autoimmune diseases. Scand. J. Immunol., 40, 636-642
17. Gatto, M., Zen, M., Ghirardello, A., Bettio, S., Bassi, N., Iaccarino, L., Punzi, L. & Doria, A. (2013) Emerging and critical issues in the pathogenesis of lupus. Autoimmun. Rev., 12, 523-536
18. Grigorian, A., Torossian, S. & Demetriou, M. (2009) T-cell growth, cell surface organization, and the galectin-glycoprotein lattice. Immunol. Rev., 230, 232-246
19. Hernandez, J.D., Nguyen, J.T., He, J., Wang, W., Ardman, B., Green, J.M., Fukuda, M. & Baum, L.G. (2006) Galectin-1 binds different CD43 glycoforms to cluster CD43 and regulate T cell death. J. Immunol., 177, 5328-5336
20. Hernández, P., Debray, H., Jaekel, H., Garfias, Y., Jiménez, Md. Mdel. C., Martínez-Cairo, S. & Zenteno, E. (2001) Chemical characterization of the lectin from Amaranthus leucocarpus syn. hypocondriacus by 2-D proteome analysis. Glycoconj. J., 18, 321-329
21. Hernández, P., Tetaert, D., Vergoten, G., Debray, H., del Carmen Jimenez, M., Fernández, G., Agundis, C., Degand, P. & Zenteno, E. (2004) Specificity of Amaranthus leucocarpus syn. hypocondriacus lectin for O-glycopeptides. Biochim. Biophys. Acta, 1674, 282-290
22. Linker-Israeli, M., Deans, R.J., Wallace, D.J., Prehn, J., Ozeri-Chen, T. & Klinenberg, J.R. (1991) Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J. Immunol., 147, 117-123
23. Liossis, S.N., Ding, X.Z., Dennis, G.J. & Tsokos, G.C. (1998) Altered pattern of TCR/CD3-mediated protein-tyrosyl phosphorylation in T cells from patients with systemic lupus erythematosus. Deficient expression of the T cell receptor zeta chain. J. Clin. Invest., 101, 1448-1457
24. Liu, Z. & Davidson, A. (2012) Taming lupus-a new understanding of pathogenesis is leading to clinical advances. Nat. Med., 18, 871-882
25. Lotan, R., Skutelsky, E., Danon, D. & Sharon, N. (1975) The purification, composition, and specificity of the anti-T lectin from peanut (Arachis hypogaea). J. Biol. Chem., 250, 8518-8523
26. Mahanta, S.K., Sastry, M.V. & Surolia, A. (1990) Topography of the combining region of a Thomsen-Friedenreich-antigenspecific lectin jacalin (Artocarpus integrifolia agglutinin). A thermodynamic and circular-dichroism spectroscopic study. Biochem. J., 265, 831-840
27. Mi, X.B. & Zeng, F.Q. (2008) Hypomethylation of interleukin-4 and-6 promoters in T cells from systemic lupus erythematosus patients. Acta Pharmacol. Sin., 29, 105-112
28. Nguyen, J.T., Evans, D.P., Galvan, M., Pace, K.E., Leitenberg, D., Bui, T.N. & Baum, L.G. (2001) CD45 modulates galectin-1-induced T cell death: regulation by expression of core 2 O-glycans. J. Immunol., 167, 5697-5707
29. Panoskaltsis, N., Reid, C.D. & Knight, S.C. (2003) Quantification and cytokine production of circulating lymphoid and myeloid cells in acute myelogenous leukaemia. Leukemia, 17, 716-730
30. Pereira, M.E., Kabat, E.A., Lotan, R. & Sharon, N. (1976) Immunochemical studies on the specificity of the peanut (Arachis hypogaea) agglutinin. Carbohydr. Res., 51, 107-118
31. Rajagopalan, S., Zordan, T., Tsokos, G.C. & Datta, S.K. (1990) Pathogenic anti-DNA autoantibody-inducing T helper cell lines from patients with active lupus nephritis: isolation of CD4-8-T helper cell lines that express the gamma delta T-cell antigen receptor. Proc. Natl. Acad. Sci. USA, 87, 7020-7024
32. Ripley, B.J., Goncalves, B., Isenberg, D.A., Latchman, D.S. & Rahman, A. (2005) Raised levels of interleukin 6 in systemic lupus erythematosus correlate with anaemia. Ann. Rheum. Dis., 64, 849-853
33. Sarkar, M., Wu, A.M. & Kabat, E.A. (1981) Immunochemical studies on the carbohydrate specificity of Maclura pomifera lectin. Arch. Biochem. Biophys., 209, 204-218
34. Sastry, M.V., Banarjee, P., Patanjali, S.R., Swamy, M.J., Swarnalatha, G.V. & Surolia, A. (1986) Analysis of saccharide binding to Artocarpus integrifolia lectin reveals specific recognition of T-antigen (beta-D-Gal(1----3)D-GalNAc). J. Biol. Chem., 261, 11726-11733
35. Shah, D., Aggarwal, A., Bhatnagar, A., Kiran, R. & Wanchu, A. (2011) Association between T lymphocyte sub-sets apoptosis and peripheral blood mononuclear cells oxidative stress in systemic lupus erythematosus. Free Radic. Res., 45, 559-567
36. Shivakumar, S., Tsokos, G.C. & Datta, S.K. (1989) T cell receptor alpha/beta expressing double-negative (CD4-/CD8-) and CD4+ T helper cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J. Immunol., 143, 103-112
37. Suzuki, H., Raska, M., Yamada, K., Moldoveanu, Z., Julian, B.A., Wyatt, R.J., Tomino, Y., Gharavi, A.G. & Novak, J. (2014) Cytokines alter IgA1 O-glycosylation by dysregulating C1GalT1 and ST6GalNAc-II enzymes. J. Biol. Chem., 289, 5330-5339
38. Swamy, M.J., Gupta, D., Mahanta, S.K. & Surolia, A. (1991) Further characterization of the saccharide specificity of peanut (Arachis hypogaea) agglutinin. Carbohydr. Res., 213, 59-67
39. Tan, E.M., Cohen, A.S, Fries, J.F., Masi, A.T., McShane, D.J., Rothfield, N.F., Schaller, J.G., Talal, N. & Winchester, R.J. (1982) The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum., 25, 1271-1277
40. The, T.H. & Feltkamp, T.E.W. (1970) Conjugation of fluorescein isothiocyanate to antibodies. I. Experiments on the conditionsof conjugation. Immunology, 18, 865-873
41. Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Zwirnerf, N.W., Poirier, F., Riley, E.M., Baum, L.G. & Rabinovich, G.A. (2007) Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol., 8, 825-834
42. Umare, V., Pradhan, V., Nadkar, M., Rajadhyaksha, A., Patwardhan, M., Ghosh, K.K. & Nadkarni, A.H. (2014) Effect of Proinflammatory Cytokines (IL-6, TNF-α, and IL-1 β) on Clinical Manifestations in Indian SLE Patients. Mediators Inflamm., 2014, 385297
43. Urrea, F., Zenteno, E., Avila-Moreno, F., Sanchez-Garcia, F.J., Zuñiga, J., Lascurain, R. & Ortiz-Quintero, B. (2011) Amaranthus leucocarpus lectin (ALL) enhances anti-CD3-dependent activation of murine T cells and promotes cell survival. Immunol. Invest., 40, 113-129
44. Vassilopoulos, D., Kovacs, B. & Tsokos, G.C. (1995) TCR/CD3 complex-mediated signal transduction pathway in T cells and T cell lines from patients with systemic lupus erythematosus. J. Immunol., 155, 2269-2281
45. Yamada, K., Kobayashi, N., Ikeda, T., Suzuki, Y., Tsuge, T., Horikoshi, S., Emancipator, S.N. & Tomino, Y. (2010) Downregulation of core 1 beta1,3-galactosyltransferase and Cosmc by Th2 cytokine alters O-glycosylation of IgA1. Nephrol. Dial. Transplant., 25, 3890-3897
46. Zenteno, E., Lascurain, R., Montaño, L.F., Vazquez, L., Debray, H. & Montreuil, J. (1992) Specificity of Amaranthus leucocarpus lectin. Glycoconj. J., 9, 204-208
47. Zenteno, E. & Ochoa, J.L. (1988) Purification of a lectin from Amaranthus leucocarpus by affinity chromatography. Phytochem., 27, 313-317.