Skip to main content

Advertisement

SpringerLink
Log in

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

  • Published:
Cellular and Molecular Bioengineering Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Aida, T., E. W. Meijer, and S. I. Stupp. Functional supramolecular polymers. Science 335:813–817, 2012.

    Article  Google Scholar 

  2. Arikawa, T., A. Matsukawa, K. Watanabe, K. M. Sakata, M. Seki, M. Nagayama, K. Takeshita, K. Ito, T. Niki, S. Oomizu, R. Shinonaga, N. Saita, and M. Hirashima. Galectin-9 accelerates transforming growth factor beta3-induced differentiation of human mesenchymal stem cells to chondrocytes. Bone 44:849–857, 2009.

    Article  Google Scholar 

  3. Ban, L., and M. Mrksich. On-chip synthesis and label-free assays of oligosaccharide arrays. Angew. Chem. Int. Edit. 47:3396–3399, 2008.

    Article  Google Scholar 

  4. Banh, A., J. Zhang, H. Cao, D. M. Bouley, S. Kwok, C. Kong, A. J. Giaccia, A. C. Koong, and Q. T. Le. Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis. Cancer Res. 71:4423–4431, 2011.

    Article  Google Scholar 

  5. Baum, L. G., D. P. Blackall, S. Arias-Magallano, D. Nanigian, S. Y. Uh, J. M. Browne, D. Hoffmann, C. E. Emmanouilides, M. C. Territo, and G. C. Baldwin. Amelioration of graft versus host disease by galectin-1. Clin. Immunol. 109:295–307, 2003.

    Article  Google Scholar 

  6. Baum, L. G., O. B. Garner, K. Schaefer, and B. Lee. Microbe–host interactions are positively and negatively regulated by galectin–glycan interactions. Front. Immunol. 5:284, 2014.

    Article  Google Scholar 

  7. Beer, M. V., C. Rech, P. Gasteier, B. Sauerzapfe, J. Salber, A. Ewald, M. Moller, L. Elling, and J. Groll. The next step in biomimetic material design: poly-LacNAc-mediated reversible exposure of extra cellular matrix components. Adv. Healthc. Mater. 2:306–311, 2013.

    Article  Google Scholar 

  8. Buskas, T., S. Ingale, and G. J. Boons. Glycopeptides as versatile tools for glycobiology. Glycobiology 16:113R–136R, 2006.

    Article  Google Scholar 

  9. Camby, I., M. Le Mercier, F. Lefranc, and R. Kiss. Galectin-1: a small protein with major functions. Glycobiology 16:137R–157R, 2006.

    Article  Google Scholar 

  10. Cedeno-Laurent, F., and C. J. Dimitroff. Galectin-1 research in T cell immunity: past, present and future. Clin. Immunol. 142:107–116, 2012.

    Article  Google Scholar 

  11. Chan, J., K. O’Donoghue, M. Gavina, Y. Torrente, N. Kennea, H. Mehmet, H. Stewart, D. J. Watt, J. E. Morgan, and N. M. Fisk. Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells 24:1879–1891, 2006.

    Article  Google Scholar 

  12. Chen, J., R. R. Pompano, F. W. Santiago, L. Maillat, R. Sciammas, T. Sun, H. Han, D. J. Topham, A. S. Chong, and J. H. Collier. The use of self-adjuvanting nanofiber vaccines to elicit high-affinity B cell responses to peptide antigens without inflammation. Biomaterials 34:8776–8785, 2013.

    Article  Google Scholar 

  13. Collier, J. H., and P. B. Messersmith. Enzymatic modification of self-assembled peptide structures with tissue transglutaminase. Bioconjug. Chem. 14:748–755, 2003.

    Article  Google Scholar 

  14. Collier, J. H., J. S. Rudra, J. Z. Gasiorowski, and J. P. Jung. Multi-component extracellular matrices based on peptide self-assembly. Chem. Soc. Rev. 39:3413–3424, 2010.

    Article  Google Scholar 

  15. Cortegano, I., V. del Pozo, B. Cardaba, B. de Andres, S. Gallardo, A. del Amo, I. Arrieta, A. Jurado, P. Palomino, F. T. Liu, and C. Lahoz. Galectin-3 down-regulates IL-5 gene expression on different cell types. J. Immunol. 161:385–389, 1998.

    Google Scholar 

  16. Du, X., J. Zhou, O. Guvench, F. O. Sangiorgi, X. Li, N. Zhou, and B. Xu. Supramolecular assemblies of a conjugate of nucleobase, amino acids, and saccharide act as agonists for proliferation of embryonic stem cells and development of zygotes. Bioconjug. Chem. 25:1031–1035, 2014.

    Article  Google Scholar 

  17. Espelt, M. V., D. O. Croci, M. L. Bacigalupo, P. Carabias, M. Manzi, M. T. Elola, M. C. Munoz, F. P. Dominici, C. Wolfenstein-Todel, G. A. Rabinovich, and M. F. Troncoso. Novel roles of galectin-1 in hepatocellular carcinoma cell adhesion, polarization, and in vivo tumor growth. Hepatology 53:2097–2106, 2011.

    Article  Google Scholar 

  18. Etulain, J., S. Negrotto, M. V. Tribulatti, D. O. Croci, J. Carabelli, O. Campetella, G. A. Rabinovich, and M. Schattner. Control of angiogenesis by galectins involves the release of platelet-derived proangiogenic factors. PLoS ONE 9:e96402, 2014.

    Article  Google Scholar 

  19. Fortuna-Costa, A., A. M. Gomes, E. O. Kozlowski, M. P. Stelling, and M. S. Pavao. Extracellular galectin-3 in tumor progression and metastasis. Front Oncol. 4:138, 2014.

    Article  Google Scholar 

  20. Friedrichs, J., A. Manninen, D. J. Muller, and J. Helenius. Galectin-3 regulates integrin alpha2beta1-mediated adhesion to collagen-I and -IV. J. Biol. Chem. 283:32264–32272, 2008.

    Article  Google Scholar 

  21. Galan, M. C., P. Dumy, and O. Renaudet. Multivalent glyco(cyclo)peptides. Chem. Soc. Rev. 42:4599–4612, 2013.

    Article  Google Scholar 

  22. Galler, K. M., L. Aulisa, K. R. Regan, R. N. D’Souza, and J. D. Hartgerink. Self-assembling multidomain peptide hydrogels: designed susceptibility to enzymatic cleavage allows enhanced cell migration and spreading. J. Am. Chem. Soc. 132:3217–3223, 2010.

    Article  Google Scholar 

  23. Garcia, I., A. Sanchez-Iglesias, M. Henriksen-Lacey, M. Grzelczak, S. Penades, and L. M. Liz-Marzan. Glycans as biofunctional ligands for gold nanorods: stability and targeting in protein-rich media. J. Am. Chem. Soc. 137:3686–3692, 2015.

    Article  Google Scholar 

  24. Gasiorowski, J. Z., and J. H. Collier. Directed intermixing in multicomponent self-assembling biomaterials. Biomacromolecules 12:3549–3558, 2011.

    Article  Google Scholar 

  25. Giano, M. C., D. J. Pochan, and J. P. Schneider. Controlled biodegradation of self-assembling beta-hairpin peptide hydrogels by proteolysis with matrix metalloproteinase-13. Biomaterials 32:6471–6477, 2011.

    Article  Google Scholar 

  26. Godula, K., and C. R. Bertozzi. Density variant glycan microarray for evaluating cross-linking of mucin-like glycoconjugates by lectins. J. Am. Chem. Soc. 134:15732–15742, 2012.

    Article  Google Scholar 

  27. Goldring, K., G. E. Jones, R. Thiagarajah, and D. J. Watt. The effect of galectin-1 on the differentiation of fibroblasts and myoblasts in vitro. J. Cell Sci. 115:355–366, 2002.

    Google Scholar 

  28. Goldstein, I. J., and R. D. Poretz. Isolation, physicochemical characterization, and carbohydrate-binding specificity of lectins. In: The Lectins: Properties, Functions, and Applications in Biology and Medicine, edited by I. E. Liener, N. Sharon, and I. J. Goldstein. Orlando: Academic Press, 1986, pp. 103–115.

    Google Scholar 

  29. Hatano, K., K. Matsuoka, and D. Terunuma. Carbosilane glycodendrimers. Chem. Soc. Rev. 42:4574–4598, 2013.

    Article  Google Scholar 

  30. Heusschen, R., A. W. Griffioen, and V. L. Thijssen. Galectin-9 in tumor biology: a jack of multiple trades. Biochim. Biophys. Acta 1836:177–185, 2013.

    Google Scholar 

  31. Horiguchi, N., K. Arimoto, A. Mizutani, Y. Endo-Ichikawa, H. Nakada, and S. Taketani. Galectin-1 induces cell adhesion to the extracellular matrix and apoptosis of non-adherent human colon cancer Colo201 cells. J. Biochem. 134:869–874, 2003.

    Article  Google Scholar 

  32. Horlacher, T., M. A. Oberli, D. B. Werz, L. Krock, S. Bufali, R. Mishra, J. Sobek, K. Simons, M. Hirashima, T. Niki, and P. H. Seeberger. Determination of carbohydrate-binding preferences of human galectins with carbohydrate microarrays. ChemBioChem 11:1563–1573, 2010.

    Article  Google Scholar 

  33. Hudalla, G. A., J. A. Modica, Y. F. Tian, J. S. Rudra, A. S. Chong, T. Sun, M. Mrksich, and J. H. Collier. A self-adjuvanting supramolecular vaccine carrying a folded protein antigen. Adv. Healthc. Mater. 2:1114–1119, 2013.

    Article  Google Scholar 

  34. Hudalla, G. A., T. Sun, J. Z. Gasiorowski, H. Han, Y. F. Tian, A. S. Chong, and J. H. Collier. Gradated assembly of multiple proteins into supramolecular nanomaterials. Nat. Mater. 13:829–836, 2014.

    Article  Google Scholar 

  35. Hughes, R. C. Galectins as modulators of cell adhesion. Biochimie 83:667–676, 2001.

    Article  Google Scholar 

  36. Ingrassia, L., I. Camby, F. Lefranc, V. Mathieu, P. Nshimyumukiza, F. Darro, and R. Kiss. Anti-galectin compounds as potential anti-cancer drugs. Curr. Med. Chem. 13:3513–3527, 2006.

    Article  Google Scholar 

  37. Ito, K., K. Stannard, E. Gabutero, A. M. Clark, S. Y. Neo, S. Onturk, H. Blanchard, and S. J. Ralph. Galectin-1 as a potent target for cancer therapy: role in the tumor microenvironment. Cancer Metastasis Rev. 31:763–778, 2012.

    Article  Google Scholar 

  38. Jiang, H. R., Z. Al Rasebi, E. Mensah-Brown, A. Shahin, D. Xu, C. S. Goodyear, S. Y. Fukada, F. T. Liu, F. Y. Liew, and M. L. Lukic. Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J. Immunol. 182:1167–1173, 2009.

    Article  Google Scholar 

  39. Jung, J. H., M. Amaike, and S. Shinkai. Sol-gel transcription of novel sugar-based superstructures composed of sugar-integrated gelators into silica: creation of a lotus-shaped silica structure. Chem. Commun. 2343–2344, 2000.

  40. Jung, J. P., A. K. Nagaraj, E. K. Fox, J. S. Rudra, J. M. Devgun, and J. H. Collier. Co-assembling peptides as defined matrices for endothelial cells. Biomaterials 30:2400–2410, 2009.

    Article  Google Scholar 

  41. Kiyonaka, S., K. Sada, I. Yoshimura, S. Shinkai, N. Kato, and I. Hamachi. Semi-wet peptide/protein array using supramolecular hydrogel. Nat. Mater. 3:58–64, 2004.

    Article  Google Scholar 

  42. Komatsu, H., S. Matsumoto, S. Tamaru, K. Kaneko, M. Ikeda, and I. Hamachi. Supramolecular hydrogel exhibiting four basic logic gate functions to fine-tune substance release. J. Am. Chem. Soc. 131:5580–5585, 2009.

    Article  Google Scholar 

  43. Kuwabara, I., and F. T. Liu. Galectin-3 promotes adhesion of human neutrophils to laminin. J. Immunol. 156:3939–3944, 1996.

    Google Scholar 

  44. Leffler, H., S. Carlsson, M. Hedlund, Y. Qian, and F. Poirier. Introduction to galectins. Glycoconj. J. 19:433–440, 2004.

    Article  Google Scholar 

  45. Lei, C. X., W. Zhang, J. P. Zhou, and Y. K. Liu. Interactions between galectin-3 and integrinbeta3 in regulating endometrial cell proliferation and adhesion. Hum. Reprod. 24:2879–2889, 2009.

    Article  Google Scholar 

  46. Levy, Y., R. Arbel-Goren, Y. R. Hadari, S. Eshhar, D. Ronen, E. Elhanany, B. Geiger, and Y. Zick. Galectin-8 functions as a matricellular modulator of cell adhesion. J. Biol. Chem. 276:31285–31295, 2001.

    Article  Google Scholar 

  47. Li, X., Y. Kuang, J. Shi, Y. Gao, H. C. Lin, and B. Xu. Multifunctional, biocompatible supramolecular hydrogelators consist only of nucleobase, amino acid, and glycoside. J. Am. Chem. Soc. 133:17513–17518, 2011.

    Article  Google Scholar 

  48. Li, X. M., Y. Kuang, and B. Xu. “Molecular trinity” for soft nanomaterials: integrating nucleobases, amino acids, and glycosides to construct multifunctional hydrogelators. Soft Matter 8:2801–2806, 2012.

    Article  Google Scholar 

  49. Loo, Y., S. Zhang, and C. A. Hauser. From short peptides to nanofibers to macromolecular assemblies in biomedicine. Biotechnol. Adv. 30:593–603, 2012.

    Article  Google Scholar 

  50. Lundquist, J. J., and E. J. Toone. The cluster glycoside effect. Chem. Rev. 102:555–578, 2002.

    Article  Google Scholar 

  51. Martinez, A., C. Ortiz Mellet, and J. M. Garcia Fernandez. Cyclodextrin-based multivalent glycodisplays: covalent and supramolecular conjugates to assess carbohydrate-protein interactions. Chem. Soc. Rev. 42:4746–4773, 2013.

    Article  Google Scholar 

  52. Miura, Y. Design and synthesis of well-defined glycopolymers for the control of biological functionalities. Polym. J. 44:679–689, 2012.

    Article  MathSciNet  Google Scholar 

  53. Moiseeva, E. P., E. L. Spring, J. H. Baron, and D. P. de Bono. Galectin 1 modulates attachment, spreading and migration of cultured vascular smooth muscle cells via interactions with cellular receptors and components of extracellular matrix. J. Vasc. Res. 36:47–58, 1999.

    Article  Google Scholar 

  54. Motran, C. C., K. M. Molinder, S. D. Liu, F. Poirier, and M. C. Miceli. Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function. Eur. J. Immunol. 38:3015–3027, 2008.

    Article  Google Scholar 

  55. Nagae, M., N. Nishi, S. Nakamura-Tsuruta, J. Hirabayashi, S. Wakatsuki, and R. Kato. Structural analysis of the human galectin-9 N-terminal carbohydrate recognition domain reveals unexpected properties that differ from the mouse orthologue. J. Mol. Biol. 375:119–135, 2008.

    Article  Google Scholar 

  56. Nagata, Y., and M. B. Burger. Wheat germ agglutinin: molecular characteristics and specificity for sugar binding. J. Biol. Chem. 249:3116–3122, 1974.

    Google Scholar 

  57. Oberg, C. T., H. Leffler, and U. J. Nilsson. Inhibition of galectins with small molecules. Chimia (Aarau) 65:18–23, 2011.

    Article  Google Scholar 

  58. Pace, K. E., H. P. Hahn, and L. G. Baum. Preparation of recombinant human galectin-1 and use in T-cell death assays. Method Enzymol. 363:499–518, 2003.

    Article  Google Scholar 

  59. Pieters, R. J. Inhibition and detection of galectins. ChemBioChem 7:721–728, 2006.

    Article  Google Scholar 

  60. Rabinovich, G. A., and M. A. Toscano. Turning ‘sweet’ on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9:338–352, 2009.

    Article  Google Scholar 

  61. Rabinovich, G. A., M. A. Toscano, S. S. Jackson, and G. R. Vasta. Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 17:513–520, 2007.

    Article  Google Scholar 

  62. Ramakrishnan, B., P. S. Shah, and P. K. Qasba. alpha-Lactalbumin (LA) stimulates milk beta-1,4-galactosyltransferase I (beta 4Gal-T1) to transfer glucose from UDP-glucose to N-acetylglucosamine. Crystal structure of beta 4Gal-T1 × LA complex with UDP-Glc. J. Biol. Chem. 276:37665–37671, 2001.

    Article  Google Scholar 

  63. Rudra, J. S., Y. F. Tian, J. P. Jung, and J. H. Collier. A self-assembling peptide acting as an immune adjuvant. Proc. Natl. Acad. Sci. USA 107:622–627, 2010.

    Article  Google Scholar 

  64. Sansone, F., and A. Casnati. Multivalent glycocalixarenes for recognition of biological macromolecules: glycocalyx mimics capable of multitasking. Chem. Soc. Rev. 42:4623–4639, 2013.

    Article  Google Scholar 

  65. Sauerzapfe, B., K. Krenek, J. Schmiedel, W. W. Wakarchuk, H. Pelantova, V. Kren, and L. Elling. Chemo-enzymatic synthesis of poly-N-acetyllactosamine (poly-LacNAc) structures and their characterization for CGL2-galectin-mediated binding of ECM glycoproteins to biomaterial surfaces. Glycoconj. J. 26:141–159, 2009.

    Article  Google Scholar 

  66. Schattner, M., and G. A. Rabinovich. Galectins: new agonists of platelet activation. Biol. Chem. 394:857–863, 2013.

    Article  Google Scholar 

  67. Shylaja, M., and H. S. Seshadri. Glycoproteins—an overview. Biochem. Educ. 17:170–178, 1989.

    Article  Google Scholar 

  68. Solis, D., M. J. Mate, M. Lohr, J. P. Ribeiro, L. Lopez-Merino, S. Andre, E. Buzamet, F. J. Canada, H. Kaltner, M. Lensch, F. M. Ruiz, G. Haroske, U. Wollina, M. Kloor, J. Kopitz, J. L. Saiz, M. Menendez, J. Jimenez-Barbero, A. Romero, and H. J. Gabius. N-domain of human adhesion/growth-regulatory galectin-9: preference for distinct conformers and non-sialylated N-glycans and detection of ligand-induced structural changes in crystal and solution. Int. J. Biochem. Cell Biol. 42:1019–1029, 2010.

    Article  Google Scholar 

  69. Stannard, K. A., P. M. Collins, K. Ito, E. M. Sullivan, S. A. Scott, E. Gabutero, I. Darren Grice, P. Low, U. J. Nilsson, H. Leffler, H. Blanchard, and S. J. Ralph. Galectin inhibitory disaccharides promote tumour immunity in a breast cancer model. Cancer Lett. 299:95–110, 2010.

    Article  Google Scholar 

  70. Stillman, B. N., D. K. Hsu, M. Pang, C. F. Brewer, P. Johnson, F. T. Liu, and L. G. Baum. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J. Immunol. 176:778–789, 2006.

    Article  Google Scholar 

  71. Stowell, S. R., C. M. Arthur, P. Mehta, K. A. Slanina, O. Blixt, H. Leffler, D. F. Smith, and R. D. Cummings. Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens. J. Biol. Chem. 283:10109–10123, 2008.

    Article  Google Scholar 

  72. Stowell, S. R., Y. Qian, S. Karmakar, N. S. Koyama, M. Dias-Baruffi, H. Leffler, R. P. McEver, and R. D. Cummings. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J. Immunol. 180:3091–3102, 2008.

    Article  Google Scholar 

  73. St-Pierre, C., H. Manya, M. Ouellet, G. F. Clark, T. Endo, M. J. Tremblay, and S. Sato. Host-soluble galectin-1 promotes HIV-1 replication through a direct interaction with glycans of viral gp120 and host CD4. J. Virol. 85:11742–11751, 2011.

    Article  Google Scholar 

  74. Sturm, A., M. Lensch, S. Andre, H. Kaltner, B. Wiedenmann, S. Rosewicz, A. U. Dignass, and H. J. Gabius. Human galectin-2: novel inducer of T cell apoptosis with distinct profile of caspase activation. J. Immunol. 173:3825–3837, 2004.

    Article  Google Scholar 

  75. Thijssen, V. L., and A. W. Griffioen. Galectin-1 and -9 in angiogenesis: a sweet couple. Glycobiology 24:915–920, 2014.

    Article  Google Scholar 

  76. Toscano, M. A., G. A. Bianco, J. M. Ilarregui, D. O. Croci, J. Correale, J. D. Hernandez, N. W. Zwirner, F. Poirier, E. M. Riley, L. G. Baum, and G. A. Rabinovich. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol. 8:825–834, 2007.

    Article  Google Scholar 

  77. Tribulatti, M. V., M. G. Figini, J. Carabelli, V. Cattaneo, and O. Campetella. Redundant and antagonistic functions of galectin-1, -3, and -8 in the elicitation of T cell responses. J. Immunol. 188:2991–2999, 2012.

    Article  Google Scholar 

  78. Wan, S. Y., T. F. Zhang, and Y. Ding. Galectin-3 enhances proliferation and angiogenesis of endothelial cells differentiated from bone marrow mesenchymal stem cells. Transplant. Proc. 43:3933–3938, 2011.

    Article  Google Scholar 

  79. Woolfson, D. N., and Z. N. Mahmoud. More than just bare scaffolds: towards multi-component and decorated fibrous biomaterials. Chem. Soc. Rev. 39:3464–3479, 2010.

    Article  Google Scholar 

  80. Yang, R. Y., D. K. Hsu, L. Yu, H. Y. Chen, and F. T. Liu. Galectin-12 is required for adipogenic signaling and adipocyte differentiation. J. Biol. Chem. 279:29761–29766, 2004.

    Article  Google Scholar 

  81. Yang, R. Y., G. A. Rabinovich, and F. T. Liu. Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 10:e17, 2008.

    Article  Google Scholar 

  82. Yu, H., H. Chokhawala, R. Karpel, B. Wu, J. Zhang, Y. Zhang, Q. Jia, and X. Chen. A multifunctional Pasteurella multocida sialyltransferase: a powerful tool for the synthesis of sialoside libraries. J. Am. Chem. Soc. 127:17618–17619, 2005.

    Article  Google Scholar 

  83. Zhou, M., A. M. Smith, A. K. Das, N. W. Hodson, R. F. Collins, R. V. Ulijn, and J. E. Gough. Self-assembled peptide-based hydrogels as scaffolds for anchorage-dependent cells. Biomaterials 30:2523–2530, 2009.

    Article  Google Scholar 

Download references

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.

Ethical Standards

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

Author information

Authors and Affiliations

  1. J. Crayton Pruitt Family Department of Biomedical Engineering, University of Florida, Biomedical Sciences J293, 1275 Center Drive, Gainesville, FL, 32611, USA

    Antonietta Restuccia & Gregory A. Hudalla

  2. Department of Surgery, University of Chicago, 5841 S. Maryland Ave. ML5032, Chicago, IL, 60637, USA

    Ye F. Tian, Joel H. Collier & Gregory A. Hudalla

  3. Department of Biomedical Engineering, Illinois Institute of Technology, Chicago, IL, USA

    Ye F. Tian

Authors
  1. Antonietta Restuccia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ye F. Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joel H. Collier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gregory A. Hudalla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

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

Additional information

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

This paper is designated as a 2014 BMES Outstanding Contribution.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12195-015-0399-2

Keywords

Search

Navigation