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Self-Assembled Glycopeptide Nanofibers as Modulators of Galectin-1 Bioactivity

Abstract

Galectins are carbohydrate-binding proteins that act as extracellular signaling molecules in various normal and pathological processes. Galectin bioactivity is mediated by specific non-covalent interactions with cell-surface and extracellular matrix glycoproteins, which can enhance or inhibit signaling events that influence various cellular behaviors, including adhesion, proliferation, differentiation, and apoptosis. Here, we developed a materials approach to modulate galectin bioactivity by mimicking natural galectin–glycoprotein interactions. Specifically, we created a variant of a peptide that self-assembles into β-sheet nanofibers under aqueous conditions, QQKFQFQFEQQ (Q11), which has an asparagine residue modified with the monosaccharide N-acetylglucosamine (GlcNAc) at its N-terminus (GlcNAc-Q11). GlcNAc-Q11 self-assembled into β-sheet nanofibers under similar conditions as Q11. Nanofibrillar GlcNAc moieties were efficiently converted to the galectin-binding disaccharide N-acetyllactosamine (LacNAc) via the enzyme β-1,4-galactosyltransferase and the sugar donor UDP-galactose, while retaining β-sheet structure and nanofiber morphology. LacNAc-Q11 nanofibers bound galectin-1 and -3 in a LacNAc concentration-dependent manner, although nanofibers bound galectin-1 with higher affinity than galectin-3. In contrast, galectin-1 bound weakly to GlcNAc-Q11 nanofibers, while no galectin-3 binding to these nanofibers was observed. Galectin-1 binding to LacNAc-Q11 nanofibers was specific because it could be inhibited by excess soluble β-lactose, a galectin-binding carbohydrate. LacNAc-Q11 nanofibers inhibited galectin-1-mediated apoptosis of Jurkat T cells in a LacNAc concentration-dependent manner, but were unable to inhibit galectin-3 activity, consistent with galectin-binding affinity of the nanofibers. We envision that glycopeptide nanofibers capable of modulating galectin-1 bioactivity will be broadly useful as biomaterials for various medical applications, including cancer therapeutics, immunotherapy, tissue regeneration, and viral prophylaxis.

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Acknowledgments

This research was supported by the National Institutes of Health (NIBIB, 1R01EB009701; NCI, U54 CA151880; NIAID, 1F32AI096769) and the National Science Foundation (DMR-1455201). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Biomedical Imaging and BioEngineering, the National Institute of Allergy and Infectious Disease, the National Cancer Institute, the National Institutes of Health, or the National Science Foundation. MALDI-TOF was performed in the University of Chicago Mass Spectrometry facility and the University of Florida Mass Spectrometry facility, with support from NSF CHE MRI 1040016. CD was performed in the University of Chicago Biophysics Core. TEM was performed in the University of Chicago Materials Research Center.

Conflict of interest

Antonietta Restuccia, Ye F. Tian, Joel H. Collier, and Gregory A. Hudalla declare that they have no conflicts of interest.

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No human studies were carried out by the authors for this article. No animal studies were carried out by the authors for this article.

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Correspondence to Joel H. Collier or Gregory A. Hudalla.

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Associate Editor Michael R. King oversaw the review of this article.

This paper is designated as a 2014 BMES Outstanding Contribution.

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Restuccia, A., Tian, Y.F., Collier, J.H. et al. Self-Assembled Glycopeptide Nanofibers as Modulators of Galectin-1 Bioactivity. Cel. Mol. Bioeng. 8, 471–487 (2015). https://doi.org/10.1007/s12195-015-0399-2

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Keywords

  • Self-assembly
  • Peptide nanofibers
  • Galectin
  • Protein–carbohydrate interactions