Glycome dynamics in T and B cell development: basic immunological mechanisms and clinical applications

Abstract

The glycosylation profile of mammalian mature T and B cells contributes to the regulation of cellular function in immune responses.The glycome of developing T and B cells shows dynamics across maturing stages.Interference in glycosylation pathways is known to lead to reprogramming of T and B cell developmental processes, often resulting in mature population defects.The relationship between glycans in T and B cell development and disease susceptibility is a promising novel research avenue. Glycans are key regulators of lymphocyte biology, highlighted by their prominent role along each T and B cell developmental stage. Further research is needed to clarify the precise contribution of these sugar chains in developmental processes and checkpoints and how this can associate with disease susceptibility for various conditions. Glycans, or carbohydrates, are present in virtually all cellular surfaces and are important regulators of the mammalian immune system (Box 1) [1.Rudd P.M. et al.Glycosylation and the immune system.Science. 2001; 291: 2370-2376Crossref PubMed Scopus (1402) Google Scholar]. Not surprisingly, T and B cells contain a dense coat of surface glycans (glycocalyx) that tightly regulate activity and function [2.Marth J.D. Grewal P.K. Mammalian glycosylation in immunity.Nat. Rev. Immunol. 2008; 8: 874-887Crossref PubMed Scopus (533) Google Scholar, 3.Pereira M.S. et al.Glycans as key checkpoints of T cell activity and function.Front. Immunol. 2018; 9: 2754Crossref PubMed Scopus (74) Google Scholar, 4.Fernandes A. et al.Glycans as shapers of tumour microenvironment: a sweet driver of T-cell-mediated anti-tumour immune response.Immunology. 2023; 168: 217-232Crossref PubMed Scopus (3) Google Scholar, 5.Alves I. et al.The role of glycosylation in inflammatory diseases.Adv. Exp. Med. Biol. 2021; 1325: 265-283Crossref PubMed Scopus (4) Google Scholar]. The composition of glycan structures within a certain cell or tissue (its glycome) contains an important amount of biological information. Glycans have been reported to be essential regulators of T and B cells [3.Pereira M.S. et al.Glycans as key checkpoints of T cell activity and function.Front. Immunol. 2018; 9: 2754Crossref PubMed Scopus (74) Google Scholar,5.Alves I. et al.The role of glycosylation in inflammatory diseases.Adv. Exp. Med. Biol. 2021; 1325: 265-283Crossref PubMed Scopus (4) Google Scholar]. Moreover, the fundamental role of glycans in immunity is vast, spanning from their impact at early stages of T and B cell development, differentiation, and selection, as well as for the B cell production of antibodies and for defining the pro- or anti-inflammatory properties of T cells. In fact, by regulating immune cell-fate decisions, activity, function, as well as early developmental processes in the thymus [2.Marth J.D. Grewal P.K. Mammalian glycosylation in immunity.Nat. Rev. Immunol. 2008; 8: 874-887Crossref PubMed Scopus (533) Google Scholar] and bone marrow [6.Ubelhart R. et al.N-linked glycosylation selectively regulates autonomous precursor BCR function.Nat. Immunol. 2010; 11: 759-765Crossref PubMed Scopus (71) Google Scholar,7.Li W. et al.Core fucosylation of mu heavy chains regulates assembly and intracellular signaling of precursor B cell receptors.J. Biol. Chem. 2012; 287: 2500-2508Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar], protein glycosylation has been implicated in most cellular processes of humoral and adaptive immunity. Early in the 1970s and 1980s, prosperous times for modern immunology, the peanut agglutinin lectin (PNA), recognizing carbohydrate sequence Gal-β(1-3)-GalNAc, was shown to differentially bind immature and mature thymocytes in mice [8.Reisner Y. et al.Separation of mouse thymocytes into two subpopulations by the use of peanut agglutinin.Cell. Immunol. 1976; 25: 129-134Crossref PubMed Scopus (384) Google Scholar]. Moreover, the binding of PNA to germinal center (GC) B cells became a standard method to identify these cells [9.Rose M.L. Malchiodi F. Binding of peanut lectin to thymic cortex and germinal centres of lymphoid tissue.Immunology. 1981; 42: 583-591PubMed Google Scholar]. These studies represent early highlights of the relevance of glycans in T and B cell development. Recent studies further demonstrated that the glycome composition of human and murine thymocytes is dynamic along different maturation stages, reigniting the hypothesis that this glycosignature is developmentally regulated [10.Vicente M.M. et al.Mannosylated glycans impair normal T-cell development by reprogramming commitment and repertoire diversity.Cell. Mol. Immunol. 2023; (Published online June 21, 2023. http://doi.org/10.1038/s41423-023-01052-7)Crossref PubMed Scopus (0) Google Scholar]. We propose that the regulation of glycan profiles is one of the mechanisms enabling normal developmental transitions that, for T and B cells, ensure proficient cellular populations adaptive and humoral immunity. In the that this further the of a glycan in T and B cell development and function and the for We present a each T and B cell developmental that the prominent role of glycans at the of humoral and adaptive immunity. 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PubMed Scopus Google Scholar]. this a prominent role of glycans in thymus is one of the in T cell development. thymic these cells into early a of the can to [10.Vicente M.M. et al.Mannosylated glycans impair normal T-cell development by reprogramming commitment and repertoire diversity.Cell. Mol. Immunol. 2023; (Published online June 21, 2023. http://doi.org/10.1038/s41423-023-01052-7)Crossref PubMed Scopus (0) Google Scholar], A. The thymic for T cells 2008; PubMed Scopus Google Scholar] The signaling is essential for T cell commitment of these immature thymocytes of the of T cell Immunol. PubMed Scopus Google Scholar]. The of the that is for murine T cell F. et T cell in mice with an of Full Text Full Text PDF PubMed Scopus Google Scholar]. are with a of glycan from as well as of glycosylation in Biol. 2010; PubMed Scopus Google Scholar]. these glycan in of their role in of in cells et the of and regulates Biol. Chem. 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