Control of intestinal inflammation by glycosylation-dependent lectin-driven immunoregulatory circuits.

Morosi, Luciano G; Cutine, Anabela M; Cagnoni, Alejandro J; Manselle-Cocco, Montana N; Croci, Diego O; Merlo, Joaquín P; Morales, Rosa M; May, María et al. · Sci Adv · 2021

basic_science · Level V

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Abstract

Diverse immunoregulatory circuits operate to preserve intestinal homeostasis and prevent inflammation. Galectin-1 (Gal1), a β-galactoside-binding protein, promotes homeostasis by reprogramming innate and adaptive immunity. Here, we identify a glycosylation-dependent "on-off" circuit driven by Gal1 and its glycosylated ligands that controls intestinal immunopathology by targeting activated CD8<sup>+</sup> T cells and shaping the cytokine profile. In patients with inflammatory bowel disease (IBD), augmented Gal1 was associated with dysregulated expression of core 2 β6-<i>N</i>-acetylglucosaminyltransferase 1 (<i>C2GNT1</i>) and α(2,6)-sialyltransferase 1 (<i>ST6GAL1</i>), glycosyltransferases responsible for creating or masking Gal1 ligands. Mice lacking Gal1 exhibited exacerbated colitis and augmented mucosal CD8<sup>+</sup> T cell activation in response to 2,4,6-trinitrobenzenesulfonic acid; this phenotype was partially ameliorated by treatment with recombinant Gal1. While <i>C2gnt1<sup>-/-</sup></i> mice exhibited aggravated colitis, <i>St6gal1<sup>-/-</sup></i> mice showed attenuated inflammation. These effects were associated with intrinsic T cell glycosylation. Thus, Gal1 and its glycosylated ligands act to preserve intestinal homeostasis by recalibrating T cell immunity.