Skip to main content
Log in

Glycobiology of the ocular surface: mucins and lectins

  • Review
  • Published:
Japanese Journal of Ophthalmology Aims and scope Submit manuscript

Abstract

Glycosylation is an important and common form of posttranscriptional modification of proteins in cells. During the last decade, a vast array of biological functions has been ascribed to glycans because of a rapid evolution in glycomic technologies. Glycogenes that are highly expressed at the human ocular surface include families of glycosyltransferases, proteoglycans, and glycan degradation proteins, as well as mucins and carbohydrate-binding proteins, such as the galectins. On the apical glycocalyx, mucin O-glycans promote boundary lubrication, prevent bacterial adhesion and endocytic activity, and maintain epithelial barrier function through interactions with galectins. The emerging roles attributed to glycans are contributing to the appreciation of their biological capabilities at the ocular surface.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /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.

Fig. 1

Similar content being viewed by others

References

  1. Varki A, Sharon N. Historical background and overview. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al., eds. Essentials of glycobiology. 2nd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2009:1–22.

  2. Bertozzi CR, Sasisekharan R. Glycomics. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al., eds. Essentials of glycobiology. 2nd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2009:633–48.

  3. Narimatsu H. Construction of a human glycogene library and comprehensive functional analysis. Glycoconj J. 2004;21:17–24.

    Article  PubMed  CAS  Google Scholar 

  4. Comelli EM, Head SR, Gilmartin T, Whisenant T, Haslam SM, North SJ, et al. A focused microarray approach to functional glycomics: transcriptional regulation of the glycome. Glycobiology. 2006;16:117–31.

    Article  PubMed  CAS  Google Scholar 

  5. Mantelli F, Schaffer L, Dana R, Head SR, Argueso P. Glycogene expression in conjunctiva of patients with dry eye: downregulation of Notch signaling. Invest Ophthalmol Vis Sci. 2009;50:2666–72.

    Article  PubMed  Google Scholar 

  6. Tanaka K, Bertolini M, Pigman W. Serine and threonine glycosidic linkages in bovine submaxillary mucin. Biochem Biophys Res Commun. 1964;16:404–9.

    Article  PubMed  CAS  Google Scholar 

  7. Guzman-Aranguez A, Mantelli F, Argueso P. Mucin-type O-glycans in tears of normal subjects and patients with non-Sjogren’s dry eye. Invest Ophthalmol Vis Sci. 2009;50:4581–7.

    Article  PubMed  Google Scholar 

  8. Bansil R, Stanley E, LaMont JT. Mucin biophysics. Annu Rev Physiol. 1995;57:635–7.

    Article  PubMed  CAS  Google Scholar 

  9. Spurr-Michaud S, Argueso P, Gipson I. Assay of mucins in human tear fluid. Exp Eye Res. 2007;84:939–50.

    Article  PubMed  CAS  Google Scholar 

  10. Berry M, Ellingham RB, Corfield AP. Human preocular mucins reflect changes in surface physiology. Br J Ophthalmol. 2004;88:377–83.

    Article  PubMed  CAS  Google Scholar 

  11. Voynow JA, Rubin BK. Mucins, mucus, and sputum. Chest. 2009;135:505–12.

    Article  PubMed  CAS  Google Scholar 

  12. Fleiszig SM, Kwong MS, Evans DJ. Modification of Pseudomonas aeruginosa interactions with corneal epithelial cells by human tear fluid. Infect Immun. 2003;71:3866–74.

    Article  PubMed  CAS  Google Scholar 

  13. Fleiszig SM, Zaidi TS, Ramphal R, Pier GB. Modulation of Pseudomonas aeruginosa adherence to the corneal surface by mucus. Infect Immun. 1994;62:1799–804.

    PubMed  CAS  Google Scholar 

  14. Aristoteli LP, Willcox MD. The adhesion of Pseudomonas aeruginosa to high molecular weight human tear film species corresponds to glycoproteins reactive with Sambucus nigra lectin. Exp Eye Res. 2006;83:1146–53. doi:10.1016/j.exer.2006.06.002.

    Article  PubMed  CAS  Google Scholar 

  15. Guzman-Aranguez A, Argueso P. Structure and biological roles of mucin-type O-glycans at the ocular surface. Ocul Surf. 2010;8:8–17.

    Article  PubMed  Google Scholar 

  16. Komatsu M, Carraway CA, Fregien NL, Carraway KL. Reversible disruption of cell-matrix and cell–cell interactions by overexpression of sialomucin complex. J Biol Chem. 1997;272:33245–54.

    Article  PubMed  CAS  Google Scholar 

  17. Bramwell ME, Wiseman G, Shotton DM. Electron-microscopic studies of the CA antigen, epitectin. J Cell Sci. 1986;86:249–61.

    PubMed  CAS  Google Scholar 

  18. Hilkens J, Ligtenberg MJ, Vos HL, Litvinov SV. Cell membrane-associated mucins and their adhesion-modulating property. Trends Biochem Sci. 1992;17:359–63.

    Article  PubMed  CAS  Google Scholar 

  19. Jentoft N. Why are proteins O-glycosylated? Trends Biochem Sci. 1990;15:291–4.

    Article  PubMed  CAS  Google Scholar 

  20. Berry M, McMaster TJ, Corfield AP, Miles MJ. Exploring the molecular adhesion of ocular mucins. Biomacromolecules. 2001;2:498–503.

    Article  PubMed  CAS  Google Scholar 

  21. Sumiyoshi M, Ricciuto J, Tisdale A, Gipson IK, Mantelli F, Argueso P. Antiadhesive character of mucin O-glycans at the apical surface of corneal epithelial cells. Invest Ophthalmol Vis Sci. 2008;49:197–203.

    Article  PubMed  Google Scholar 

  22. Shogren R, Gerken TA, Jentoft N. Role of glycosylation on the conformation and chain dimensions of O-linked glycoproteins: light-scattering studies of ovine submaxillary mucin. Biochemistry. 1989;28:5525–36.

    Article  PubMed  CAS  Google Scholar 

  23. Ciborowski P, Finn OJ. Non-glycosylated tandem repeats of MUC1 facilitate attachment of breast tumor cells to normal human lung tissue and immobilized extracellular matrix proteins (ECM) in vitro: potential role in metastasis. Clin Exp Metastasis. 2002;19:339–45.

    Article  PubMed  CAS  Google Scholar 

  24. Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, Hauck CR. Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci. 2005;118:2189–200.

    Article  PubMed  CAS  Google Scholar 

  25. Hauck CR, Agerer F, Muenzner P, Schmitter T. Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol. 2006;85:235–42.

    Article  PubMed  CAS  Google Scholar 

  26. Jett BD, Gilmore MS. Host–parasite interactions in Staphylococcus aureus keratitis. DNA Cell Biol. 2002;21:397–404.

    Article  PubMed  CAS  Google Scholar 

  27. Ricciuto J, Heimer SR, Gilmore MS, Argueso P. Cell surface O-glycans limit Staphylococcus aureus adherence to corneal epithelial cells. Infect Immun. 2008;76:5215–20.

    Article  PubMed  CAS  Google Scholar 

  28. Argueso P, Sumiyoshi M. Characterization of a carbohydrate epitope defined by the monoclonal antibody H185: sialic acid O-acetylation on epithelial cell-surface mucins. Glycobiology. 2006;16:1219–28.

    Article  PubMed  CAS  Google Scholar 

  29. Argueso P, Spurr-Michaud S, Russo CL, Tisdale A, Gipson IK. MUC16 mucin is expressed by the human ocular surface epithelia and carries the H185 carbohydrate epitope. Invest Ophthalmol Vis Sci. 2003;44:2487–95.

    Article  PubMed  Google Scholar 

  30. Williamson YM, Gowrisankar R, Longo DL, Facklam R, Gipson IK, Ades EP, et al. Adherence of nontypeable Streptococcus pneumoniae to human conjunctival epithelial cells. Microb Pathog. 2008;44:175–85.

    Article  PubMed  CAS  Google Scholar 

  31. Cao Z, Said N, Amin S, Wu HK, Bruce A, Garate M, et al. Galectins-3 and -7, but not galectin-1, play a role in re-epithelialization of wounds. J Biol Chem. 2002;277:42299–305.

    Article  PubMed  CAS  Google Scholar 

  32. Gupta SK, Masinick S, Garrett M, Hazlett LD. Pseudomonas aeruginosa lipopolysaccharide binds galectin-3 and other human corneal epithelial proteins. Infect Immun. 1997;65:2747–53.

    PubMed  CAS  Google Scholar 

  33. Hrdlickova-Cela E, Plzak J, Smetana K Jr, Melkova Z, Kaltner H, Filipec M, et al. Detection of galectin-3 in tear fluid at disease states and immunohistochemical and lectin histochemical analysis in human corneal and conjunctival epithelium. Br J Ophthalmol. 2001;85:1336–40.

    Article  PubMed  CAS  Google Scholar 

  34. Dumic J, Dabelic S, Flogel M. Galectin-3: an open-ended story. Biochim Biophys Acta. 2006;1760:616–35.

    Article  PubMed  CAS  Google Scholar 

  35. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, et al. Galectins: a family of animal beta-galactoside-binding lectins. Cell. 1994;76:597–8.

    Article  PubMed  CAS  Google Scholar 

  36. Ahmad N, Gabius HJ, Andre S, Kaltner H, Sabesan S, Roy R, et al. Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem. 2004;279:10841–7.

    Article  PubMed  CAS  Google Scholar 

  37. Lepur A, Salomonsson E, Nilsson UJ, Leffler H. Ligand induced galectin-3 protein self-association. J Biol Chem. 2012;287:21751–6.

    Article  PubMed  CAS  Google Scholar 

  38. Nieminen J, Kuno A, Hirabayashi J, Sato S. Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J Biol Chem. 2007;282:1374–83.

    Article  PubMed  CAS  Google Scholar 

  39. Argueso P, Guzman-Aranguez A, Mantelli F, Cao Z, Ricciuto J, Panjwani N. Association of cell surface mucins with galectin-3 contributes to the ocular surface epithelial barrier. J Biol Chem. 2009;284:23037–45.

    Article  PubMed  Google Scholar 

  40. van der Bijl P, van Eyk AD. Human vaginal mucosa as a model of buccal mucosa for in vitro permeability studies: an overview. Curr Drug Deliv. 2004;1:129–35.

    Article  PubMed  Google Scholar 

  41. Thoft RA, Friend J. Permeability of regenerated corneal epithelium. Exp Eye Res. 1975;21:409–16.

    Article  PubMed  CAS  Google Scholar 

  42. Shah A, Farooq AV, Tiwari V, Kim MJ, Shukla D. HSV-1 infection of human corneal epithelial cells: receptor-mediated entry and trends of re-infection. Mol Vis. 2010;16:2476–86.

    PubMed  CAS  Google Scholar 

  43. Yamamoto N, Petroll MW, Cavanagh HD, Jester JV. Internalization of Pseudomonas aeruginosa is mediated by lipid rafts in contact lens-wearing rabbit and cultured human corneal epithelial cells. Invest Ophthalmol Vis Sci. 2005;46:1348–55.

    Article  PubMed  Google Scholar 

  44. Guzman-Aranguez A, Woodward AM, Pintor J, Argueso P. Targeted disruption of core 1 beta1,3-galactosyltransferase (C1galt1) induces apical endocytic trafficking in human corneal keratinocytes. PLoS ONE. 2012;7:e36628. doi:10.1371/journal.pone.0036628.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial support was provided by NIH grant R01EY014847.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pablo Argüeso.

About this article

Cite this article

Argüeso, P. Glycobiology of the ocular surface: mucins and lectins. Jpn J Ophthalmol 57, 150–155 (2013). https://doi.org/10.1007/s10384-012-0228-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10384-012-0228-2

Keywords

Navigation