Galectin-3 type-C self-association on neutrophil surfaces; The carbohydrate recognition domain regulates cell function

J Leukoc Biol. 2018 Feb;103(2):341-353. doi: 10.1002/JLB.3A0317-110R. Epub 2018 Jan 10.

Abstract

Galectin-3 is an endogenous β-galactoside-binding lectin comprising a carbohydrate recognition domain (CRD) linked to a collagen-like N-domain. Both domains are required for galectin-3 to induce cellular effects; a C-terminal fragment of galectin-3, galectin-3C, containing the CRD but lacking the N-domain, binds cell surface glycoconjugates but does not induce cellular effects since cross-linking promoted by the N-domain is thought to be required. Instead, galectin-3C is proposed to antagonize the effects of galectin-3 by competing for binding sites. The aim of this study was to investigate the effects of galectin-3C on galectin-3 interactions with human neutrophils. Recombinant galectin-3C inhibited galectin-3-induced production of reactive oxygen species in primed neutrophils. Surprisingly, this inhibition was not due to competitive inhibition of galectin-3 binding to the cells. In contrast, galectin-3C potentiated galectin-3 binding, in line with emerging evidence that galectin-3 can aggregate not only through the N-domain but also through the CRD. The cell surface interaction between galectin-3C and galectin-3 was corroborated by colocalization of fluorescently labeled galectin-3 and galectin-3C. Galectin-3C can be generated in vivo through cleavage of galectin-3 by proteases. Indeed, in circulation, galectin-3 and galectin-3C were both attached to the cell surface of neutrophils, which displayed great capacity to bind additional galectin-3 and galectin-3C. In conclusion, galectin-3C enhances galectin-3 binding to neutrophils by nonactivating type-C self-association, in parallel to inhibiting neutrophil activation by galectin-3 (induced by type-N self-association). This implicates type-C self-association as a termination system for galectin-3-induced cell activation, with the purpose of avoiding oxidant-dependent tissue damage.

Keywords: ROS production; carbohydrate recognition domain; galectin; neutrophils; priming.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Blood Proteins
  • Fluorescence
  • Galactosides / metabolism*
  • Galectin 3 / genetics
  • Galectin 3 / metabolism*
  • Galectins
  • Humans
  • Leukocytes, Mononuclear / metabolism
  • NADP / metabolism
  • Neutrophils / metabolism*
  • Oxidoreductases / metabolism
  • Protein Binding
  • Reactive Oxygen Species / metabolism
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism

Substances

  • Blood Proteins
  • Galactosides
  • Galectin 3
  • Galectins
  • LGALS3 protein, human
  • Reactive Oxygen Species
  • Recombinant Proteins
  • beta-galactoside
  • NADP
  • Oxidoreductases