Neurochemical Research

, Volume 31, Issue 5, pp 619–628 | Cite as

Differential Binding to Glycotopes Among the Layers of Three Mammalian Retinal Neurons by Man-Containing N-linked Glycan, Tα (Galβ1–3GalNAcα1-), Tn (GalNAcα1-Ser/Thr) and Iβ/IIβ (Galβ1–3/4GlcNAcβ-) Reactive Lectins

  • Wei-Chi Wu
  • Chi-Chun Lai
  • Jia-Hau Liu
  • Tanuja Singh
  • Lien-Ming Li
  • Willy J. Peumans
  • Els J. M. Van Damme
  • Albert M. Wu


Carbohydrate structures between retinal neurons and retinal pigment epithelium (RPE) play an important role in maintaining the integrity of retinal adhesion to underlying RPE, and in retinal detachment pathogenesis. Since relevant knowledge is still in the primary stage, glycotopes on the adult retina of mongrel canines (dog), micropigs and Sprague-Dawley rats were examined by lectino-histochemistry, using a panel of 16 different lectins. Paraffin sections of eyes were stained with biotinylated lectins, and visualized by streptavidin-peroxidase and diaminobenzidine staining. Mapping the affinity profiles, it is concluded that: (i) all sections of the retina reacted well with Morniga M, suggesting that N-linked glycans are present in all layers of the retina; (ii) no detectable human blood group ABH active glycotopes were found among retinal layers; (iii) outer and inner segments contained glycoconjugates rich in ligands reacting with T α (Galβ1–3GalNAcα1-Ser/Thr) and Tn (GalNAcα1-Ser/Thr) specific lectins; (iv) cone cells of retina specifically bound peanut agglutinin (PNA), which recognizes T α residues and could be used as a specific marker for these photoreceptors; (v) the retinas of rat, dog and pig, had a similar binding profile but with different intensity; (vi) each retinal layer had its own binding characteristic. This information may provide useful background knowledge for normal retinal physiology and miscellaneous retinal diseases, including retinal detachment (RD) and age-related macular degeneration (ARMD).


Carbohydrate Disaccharide structural units Lectins Retina 



This study was supported by grants from National Science Council, Taiwan (NSC 94-2320-B-182-044, NSC 94-2320-B-182-053). This work was also supported by grants from the Chang-Gung Medical Research Project (CMRPD no. 33022, Kwei-san, Tao-yuan, Taiwan) and grants from the Fund for Scientific Research-Flanders (to E.J.M. Van Damme).


  1. 1.
    Blanks JC (2001) Morphology and topography of the retina. In: Ryan SJ, Odgen TE, Hinton DR (eds) Basic science and inherited retinal disease. Mosby, St. Louis, pp 32–53Google Scholar
  2. 2.
    Silver FH, Benedetto D (1996) Polysaccharides used in ophthalmology. In: Dimitriu S (ed) Polysaccharides in medicine and biotechnology Marcel Dekker, New York, pp 689–703Google Scholar
  3. 3.
    Lazarus HS, Hageman GS (1992) Xyloside-induced disruption of interphotoreceptor matrix proteoglycans results in retinal detachment. Invest Ophthalmol Vis Sci 33:364–376PubMedGoogle Scholar
  4. 4.
    Wu AM (2001) Expression of binding properties of Gal/GalNAc reactive lectins by mammalian glycotopes. Adv Exp Med Biol 491:55–64PubMedGoogle Scholar
  5. 5.
    Wu AM, Song SC, Tsai MS, Herp A (2001) A guide to the carbohydrate specificities of applied lectins-2. Adv Exp Med Biol 491:551–585PubMedGoogle Scholar
  6. 6.
    Wu AM, Wu JH, Singh T, Chu KC, Peumans WJ, Rougé P, Van Damme EJM (2004) A novel lectin (Morniga M) from mulberry (Morus nigra) bark recognizes oligomannosyl residues in N-glycans. J Biomed Sci 11:874–885PubMedGoogle Scholar
  7. 7.
    Sarkar M, Wu AM, Kabat EA (1981) Immunochemical studies on the carbohydrate specificity of Maclura pomifera lectin. Arch Biochem Biophys 209:204–218CrossRefPubMedGoogle Scholar
  8. 8.
    Duk M, Lisowska E, Wu JH, Wu AM (1994) The biotin/avidin-mediated microtiter plate lectin assay with the use of chemically modified glycoprotein ligand. Anal Biochem 221:266–272CrossRefPubMedGoogle Scholar
  9. 9.
    Wu AM (2003) Carbohydrate structural units in glycoproteins and polysaccharides as important ligands for Gal and GalNAc reactive lectins. J Biomed Sci 10:676–688PubMedCrossRefGoogle Scholar
  10. 10.
    Wu AM (2004) Polyvalency of Tn (GalNAcα→Ser/Thr) glycotope as a critical factor for Vicia villosa B4 and glycoprotein interactions. FEBS Lett 562:51–58CrossRefPubMedGoogle Scholar
  11. 11.
    Gabius HJ, Gabius S (1993) Lectins as tools for the characterization of glycoconjugates and lectins and neoglycoconjugates in histochemical and cytochemical analysis. In: Gabius HJ, Gabius S (eds) Lectins and glycobiology. Springer, Berlin, pp 141–187 and 211–326Google Scholar
  12. 12.
    Sharon N, Lis H (eds) (2003) Lectins. Kluwer Academic Publishers, Dordrecht, Boston, LondonGoogle Scholar
  13. 13.
    Hakomori S, Kannagi R (1986) Handbook of experimental immunology. In: Weir DM (ed) Immunochemistry. Blackwell Scientific Oxford, London and Boston, pp 9.1–9.39Google Scholar
  14. 14.
    Sameshima M, Uehara F, Ohba N (1987) Specialization of the interphotoreceptor matrices around cone and rod photoreceptor cells in the monkey retina, as revealed by lectin cytochemistry. Exp Eye Res 45:845–863PubMedCrossRefGoogle Scholar
  15. 15.
    Wu AM, Sugii S (1988) Differential binding properties of GalNAc and/or Gal specific lectins. Adv Exp Med Biol 228:205–263PubMedGoogle Scholar
  16. 16.
    Bishop PN, Boulton M, McLeod D, Stoddart RW (1993) Glycan localization within the human interphotoreceptor matrix and photoreceptor inner and outer segments. Glycobiology 3:403–412PubMedCrossRefGoogle Scholar
  17. 17.
    Blanks JC, Johnson LV (1983) Selective lectin binding of the developing mouse retina. J Comp Neurol 221:31–41CrossRefPubMedGoogle Scholar
  18. 18.
    Bopp S, el-Hifnawi ES, Laqua H (1992) Lectin binding pattern in human retinal pigment epithelium. Anat Anz 174:279–285Google Scholar
  19. 19.
    Kivela T, Tarkkanen A (1987) A lectin cytochemical study of glycoconjugates in the human retina. Cell Tissue Res 249:277–288PubMedCrossRefGoogle Scholar
  20. 20.
    Koide H, Suganuma T, Murata F, Ohba N (1986) Ultrastructural localization of lectin receptors in the monkey retinal photoreceptors and pigment epithelium: application of lectin-gold complexes on thin sections. Exp Eye Res 43:343–354PubMedCrossRefGoogle Scholar
  21. 21.
    McLaughlin BJ, Boykins LG (1984) Lectin cytochemistry and freeze-fracture study of phagocytosis in the rat retina. J Comp Neurol 223:77–87CrossRefPubMedGoogle Scholar
  22. 22.
    Uehara F, Ohba N, Sameshima M, Unoki K, Okubo A, Yanagita T, Sugata M, Iwakiri N, Nakagawa S (1994) Binding of amaranthin in photoreceptors of monkey retina. Jpn J Ophthalmol 38:360–363PubMedGoogle Scholar
  23. 23.
    Yan Q, Bumsted K, Hendrickson A (1995) Differential peanut agglutinin lectin labeling for S and L/M cone matrix sheaths in adult primate retina. Exp Eye Res 61:763–766CrossRefPubMedGoogle Scholar
  24. 24.
    Lazarus HS, Sly WS, Kyle JW, Hageman GS (1993) Photoreceptor degeneration and altered distribution of interphotoreceptor matrix proteoglycans in the mucopolysaccharidosis VII mouse. Exp Eye Res 56:531–541CrossRefPubMedGoogle Scholar
  25. 25.
    Long KO, Aguirre GD (1991) The cone matrix sheath in the normal and diseased retina: cytochemical and biochemical studies of peanut agglutinin-binding proteins in cone and rod-cone degeneration. Exp Eye Res 52:699–713CrossRefPubMedGoogle Scholar
  26. 26.
    McLaughlin BJ, Wood JG (1980) The localization of lectin binding sites on photoreceptor outer segments and pigment epithelium of dystrophic retinas. Invest Ophthalmol Vis Sci 19:728–742PubMedGoogle Scholar
  27. 27.
    Mieziewska K, Van Veen T, Aguirre GD (1993) Development and fate of interphotoreceptor matrix components during dysplastic photoreceptor differentiation: a lectin cytochemical study of rod-cone dysplasia 1. Exp Eye Res 56:429–441CrossRefPubMedGoogle Scholar
  28. 28.
    Mieziewska K, Van Veen T, Aguirre GD (1993) Structural changes of the interphotoreceptor matrix in an inherited retinal degeneration: a lectin cytochemical study of progressive rod-cone degeneration. Invest Ophthalmol Vis Sci 34:3056–3067PubMedGoogle Scholar
  29. 29.
    Kivela T 1987 Glycoconjugates in retinoblastoma. A lectin histochemical study of ten formalin-fixed and paraffin-embedded tumours. Virchows Arch A Pathol Anat Histopathol 410:471–479PubMedCrossRefGoogle Scholar
  30. 30.
    Lee RT, Lee YC (2000) Affinity enhancement by multivalent lectin-carbohydrate interaction. Glycoconj J 17:543–551CrossRefPubMedGoogle Scholar
  31. 31.
    Wu AM, Wu JH, Herp A, Liu JH (2003) Effect of polyvalencies of glycotopes on the binding of a lectin from the edible mushroom, Agaricus bisporus. Biochem J 371:311–320CrossRefPubMedGoogle Scholar
  32. 32.
    Lewis H (2003) Peripheral retinal degenerations and the risk of retinal detachment. Am J Ophthalmol 136:155–160CrossRefPubMedGoogle Scholar
  33. 33.
    The Eye Disease Case-Control Study Group (1993) Risk factors for idiopathic rhegmatogenous retinal detachment. Am J Epidemiol 137:749–757Google Scholar
  34. 34.
    Hageman GS, Johnson LV (1987) Chondroitin 6-sulfate glycosaminoglycan is a major constituent of primate cone photoreceptor matrix sheaths. Curr Eye Res 6:639–646PubMedCrossRefGoogle Scholar
  35. 35.
    Hollyfield JG, Varner HH, Rayborn ME (1990) Regional variation within the interphotoreceptor matrix from fovea to the retinal periphery. Eye 4:333–339PubMedGoogle Scholar
  36. 36.
    Lazarus HS, Hageman GS (1992) Xyloside-induced disruption of interphotoreceptor matrix proteoglycans results in retinal detachment. Invest Ophthalmol Vis Sci 33:364–736PubMedGoogle Scholar
  37. 37.
    Mintz G, Gottlieb DI, Reitman ML et al (1981) Developmental changes in glycoproteins of the chick nervous system. Brain Res 206:51–70CrossRefPubMedGoogle Scholar
  38. 38.
    Russell SR, Mullins RF, Schneider BL, Hageman GS (2000) Location, substructure, and composition of basal laminar drusen compared with drusen associated with aging and age-related macular degeneration. Am J Ophthalmol 129:205–214CrossRefPubMedGoogle Scholar
  39. 39.
    Yamashita T, Uehara F, Ozawa M, Ohba N (2002) Further characterization of human mucin-like glycoprotein associated with photoreceptor cells by its introduction into Y79 retinoblastoma cells. Ophthalmic Res 34:70–76CrossRefPubMedGoogle Scholar
  40. 40.
    Wu AM, Wu JH, Lin LH, Lin SH, Liu JH (2003) Binding profile of Artocarpus integrifolia agglutinin (Jacalin). Life Sci 72:2285–2302CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Wei-Chi Wu
    • 1
  • Chi-Chun Lai
    • 1
  • Jia-Hau Liu
    • 1
  • Tanuja Singh
    • 2
  • Lien-Ming Li
    • 1
  • Willy J. Peumans
    • 3
  • Els J. M. Van Damme
    • 3
  • Albert M. Wu
    • 2
  1. 1.Department of OphthalmologyChang Gung Memorial HospitalTao-yuanTaiwan
  2. 2.Glyco-Immunochemistry Research Laboratory, Institute of Molecular and Cellular BiologyChang-Gung UniversityTao-yuanTaiwan
  3. 3.Department of Molecular Biotechnology, Faculty of Bioscience EngineeringGhent UniversityGentBelgium

Personalised recommendations