Skip to main content
SpringerLink
Log in

Expression pattern of Glycoconjugates in Rat Retina as Analysed by Lectin Histochemistry

  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Abstract

The present study sought to characterize the expression and distribution of complex glycoconjugates in the rat retina by lectin histochemistry, using a panel of 21 different lectins with different carbohydrate specificities. Paraffin sections of Carnoy-fixed Sprague–Dawley rat eyes were stained with various biotinylated lectins, followed by the streptavidin-peroxidase and glucose oxidase–diaminobenzidine–nickel staining procedures. The results showed that the retinal pigment epithelium was stained intensely with LCA, Jacalin, WFA, S-WGA, PWA, DSA, UEA-I, LTA and PHA-E, suggesting that this epithelium contained glycoconjugates with α-Man, α-Glc, α-Gal/GalNAc, β-GalNAc, α-Fuc, NeuAc and other oligosaccharide residues. The outer and inner segments of the photoreceptor layer showed different lectin binding affinities. The outer segments reacted with S-WGA and GS-II, whereas the inner segments reacted with UEA-II, UEA-I, LTA and MAA, suggesting that the inner segments contained glycoconjugates rich in α-Fuc and NeuAc(α2,3)Gal residues. PNA labelled specifically the cones and could be used as a specific marker for these photoreceptors. RCA-I, WFA, S-WGA, DSA, MAA and PHA-E reacted with both the outer and inner plexiform layers. On the other hand, UEA-I and LTA specifically labelled the outer plexiform layer, while PNA labelled the inner plexiform layer. The retinal microglial cells were labelled specifically by GS-I-B4 and SNA. Interestingly, we also observed that WFA bound specifically to Müller cells and could be used as a novel marker for this retinal glial cell. The capillaries and larger vessels in the retina and choriocapillaris reacted intensely with GS-I-B4, RCA-I, S-WGA, PWA, DSA and PHA-E. No significant differences in lectin binding were observed in the microvessels at these two sites. In summary, the present study demonstrated the expression patterns of glycoconjugates in the rat retina and that certain lectins could be used as histochemical markers for specific structural and cellular components of the rat retina.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arregui C, Barra HS, Landa CA (1992) Peanut agglutinin binding glycoproteins in the chicken retina: Their presence in Müller glia cells. J Neurosci Res 31: 532–542.

    Article  CAS  PubMed  Google Scholar 

  • Ashwell K (1989) Development of microglia in the albino rabbit retina. J Comp Neurol 187: 286–301.

    Article  Google Scholar 

  • Ashwell K, Hollander H, Streit W, Stone J (1989) The appearance and distribution of microglia in the developing retina of the rat.Vis Neurosci 2: 437–448.

    Article  CAS  PubMed  Google Scholar 

  • Bee JA (1982) Glycoconjugates of the avian eye: The development and maturation of the neural retina as visualized by lectin binding. Differentiation 23: 128–140.

    Article  CAS  PubMed  Google Scholar 

  • Bishop PN, Boulton M, McLeod D, Stoddart RW (1993) Glycan localization within the human interphotoreceptor matrix and photoreceptor inner and outer segments. Glycobiology 3: 403–412.

    Article  CAS  PubMed  Google Scholar 

  • Blanks JC, Johnson LV (1984) Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Invest Ophthalmol Vis Sci 25: 546–557.

    CAS  PubMed  Google Scholar 

  • Blanks JC, Johnson LV (1983) Selective lectin binding of the developing mouse retina. J Comp Neurol 221: 31–41.

    Article  CAS  PubMed  Google Scholar 

  • Bopp S, El-Hifnawi E, Laqua H (1992) Lectin binding pattern in human retinal pigment epithelium. Ann Anat 174: 279–285.

    CAS  PubMed  Google Scholar 

  • Bridges CDB (1981) Lectin receptors of rods and cones. Visualization by fluorescent label. Invest Ophthalmol Vis Sci 20: 8–16.

    CAS  PubMed  Google Scholar 

  • Bridges CDB, Fong SL (1980) Lectin receptors on rod and cone membranes. Photochem Photobiol 32: 481–486.

    Article  CAS  PubMed  Google Scholar 

  • Bridges CDB, Fong SL (1979) Different receptors for distribution of peanut and ricin agglutinins between inner and outer segments of rod cells. Nature 282: 513–515.

    Article  CAS  PubMed  Google Scholar 

  • Chan FL, Choi HL (1995) Proteoglycans associated with the ciliary zonule of the rat eye:Ahistochemical and immunohistochemical study. Histochem Cell Biol 104: 369–381.

    Article  CAS  PubMed  Google Scholar 

  • Chan FL, Poon HK, Huang Y, Choi HL (1999) Glycoconjugates of the rat ciliary body epithelium: A lectin histochemical and protein blotting study. Histochem J 31: 95–107.

    Article  CAS  PubMed  Google Scholar 

  • Chan L, Wong YC (1991) Glycoconjugates of the lateral prostate of the guinea pig: A lectin histochemical study. Prostate 19: 155–172.

    Article  CAS  PubMed  Google Scholar 

  • Cohen D, Nir I (1987) Cytochemical characterization of sialoglycoconjugates on rat photoreceptor cell surface. Invest Ophthalmol Vis Sci 28: 640–645.

    CAS  PubMed  Google Scholar 

  • Damjanov I (1987) Lectin cytochemistry and histochemistry. Lab Invest 57: 5–20.

    CAS  PubMed  Google Scholar 

  • Debray H, Decout D, Strecker G, Spik G, Montreuil J (1981) Specificity of twelve lectins towards oligosaccharides and glycopeptides relate to N-glycosylproteins. Eur J Biochem 117: 41–55.

    Article  CAS  PubMed  Google Scholar 

  • Gariano RF, Iruela-Arispe ML, Sage EH, Hendrickson AE (1996) Immunohistochemical characterization of developing and mature primate retinal blood vessels. Invest Ophthalmol Vis Sci 37: 93–103.

    CAS  PubMed  Google Scholar 

  • Gerard C (1990) Purification of glycoproteins. Methods Enzymol 182: 529–539.

    Article  CAS  PubMed  Google Scholar 

  • Goldstein IJ, Poretz RD (1986) Isolation, physiochemical characterization, and carbohydrate-binding specificity of lectins. In: Liener IE, Sharon N, Goldstein IJ, eds. The Lectins. Properties, Functions, and Applications in Biology and Medicine. Academic Press: Orlando, pp. 33–247.

    Google Scholar 

  • Hageman GS, Johnson LV (1986) Biochemical characterization of the major peanut-agglutinin-binding glycoproteins in vertebrate retinae. J Comp Neurol 249: 499–510.

    Article  CAS  PubMed  Google Scholar 

  • Hall MO, Nir I (1976) The binding of Concanavalin A to the rod outer segments and pigment epithelium of normal and RCS rats. Exp Eye Res 22: 469–476.

    Article  CAS  PubMed  Google Scholar 

  • Hicks D, Barnstable CJ (1986) Lectin and antibody labelling of developing rat photoreceptor cells: An electron microscope immunocytochemical study. J Neurocytol 15: 219–230.

    Article  CAS  PubMed  Google Scholar 

  • Hicks D, Molday RS (1985) Localization of lectin receptors on bovine photoreceptor cells using dextran-gold markers. Invest Ophthalmol Vis Sci 26: 1002–1013.

    CAS  PubMed  Google Scholar 

  • Hogan MJ, Alvarado JA, Weddell JE (1971) Histology of the Human Eye. Saunders: Philadelphia, WB.

    Google Scholar 

  • Johnson LV, Hageman GS (1987) Enzymatic characterization of peanut agglutinin-binding components in the retinal interphotoreceptor matrix. Exp Eye Res 44: 553–565.

    Article  CAS  PubMed  Google Scholar 

  • Johnson LV, Hageman GS, Blanks JC (1986) Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest Ophthalmol Vis Sci 27: 129–135.

    CAS  PubMed  Google Scholar 

  • Kivelä T (1990) Characterization of galactose-containing glycoconjugates in the human retina: A lectin histochemical study. Curr Eye Res 9: 1195–1209.

    Article  PubMed  Google Scholar 

  • Kivelä T, Tarkkanen A (1987) A lectin cytochemical study of glycoconjugates in the human retina. Cell Tissue Res 249: 277–288.

    Article  PubMed  Google Scholar 

  • Kivelä T (1987) Glycoconjugates in retinoblastoma. A lectin histochemical study of ten formalin-fixed and paraffin-embedded tumours. Virchows Arch A Pathol Anat Histopathol 410: 471–479.

    Article  PubMed  Google Scholar 

  • 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: 343–354.

    Article  CAS  PubMed  Google Scholar 

  • Lawrenson JG, Cassella JP, Hayes AJ, Firth JA, Allt G (2000) Endothelial glycoconjugates: A comparative lectin study of the brain, retina and myocardium. J Anat 196: 55–60.

    Article  CAS  PubMed  Google Scholar 

  • 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: 531–541.

    Article  CAS  PubMed  Google Scholar 

  • Lis H, Sharon N (1986) Lectins as molecules and as tools. Annu Rev Biochem 55: 35–67.

    Article  CAS  PubMed  Google Scholar 

  • 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 cone-rod degeneration. Exp Eye Res 52: 699–713.

    Article  CAS  PubMed  Google Scholar 

  • Ma N, Streilein JW (1998) Contribution of microglia as passenger leukocytes to the fate of intraocular neuronal retinal grafts. Invest Ophthalmol Vis Sci 39: 2384–2393.

    CAS  PubMed  Google Scholar 

  • McLaughlin BJ, Boykins LG, Caldwell RB (1984) Lectin-ferritin binding on dystrophic and normal retinal pigment epithelial membranes. J Neurocytol 13: 467–480.

    Article  CAS  PubMed  Google Scholar 

  • 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: 728–742.

    CAS  PubMed  Google Scholar 

  • McLaughlin BJ, Wood JG, Gurd JW (1980) The localization of lectin binding sites during photoreceptor synaptogenesis in the chick retina. Brain Res 191: 345–357.

    Article  CAS  PubMed  Google Scholar 

  • 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: 3056–3067.

    CAS  PubMed  Google Scholar 

  • Mieziewska K, van Veen T, Aguirre GD (1993) Development and fate of interphotoreceptor matrix components during dysplastic photoreceptor differentiation:Alectin cytochemical study of rod-cone dysplasia 1. Exp Eye Res 56: 429–441.

    Article  CAS  PubMed  Google Scholar 

  • Molday LL, Molday RS (1987) Glycoproteins specific for the retinal rod outer segment plasma membrane. Biochim Biophys Acta 897: 335–340.

    Article  CAS  PubMed  Google Scholar 

  • Molday RS (1976) A scanning electron microscope study of Concanavalin A receptors on retinal rod cells labeled with latex microspheres. J Supramol Struct 4: 549–557.

    Article  CAS  PubMed  Google Scholar 

  • Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, Nielsen S, Agre P, Ottersen OP (1998) Aquaporin-4 water channel protein in the rat retina and optic nerve: Polarized expression inMüller cells and fibrous astrocytes. J Neurosci 18: 2506–2519.

    CAS  PubMed  Google Scholar 

  • Nir I, Cohen D (1987) Surface glycoconjugates on rat photoreceptor cilium. Invest Ophthalmol Vis Sci 28: 1070–1077.

    CAS  PubMed  Google Scholar 

  • Nir I, Hall MO (1979) Ultrastructural localization of lectin binding sites on the surface of retinal photoreceptors and pigment epithelium. Exp Eye Res 29: 181–194.

    Article  CAS  PubMed  Google Scholar 

  • Roque RS, Caldwell RB (1993) Isolation and culture of retinal microglia. Curr Eye Res 12: 285–290.

    Article  CAS  PubMed  Google Scholar 

  • Russell SR, Shepherd JD, Hageman GS (1991) Distribution of glycoconjugates in the human retinal lateral limiting membrane. Invest Ophthalmol Vis Sci 32: 1986–1995.

    CAS  PubMed  Google Scholar 

  • 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: 845–863.

    Article  CAS  PubMed  Google Scholar 

  • Schumacher U, Adam E, Kretzschmar H, Pfüller U (1994) Binding patterns of mistletoe lectins I, II and III to microglia and Alzheimer plaque glycoproteins in human brains. Acta Histochem 96: 399–403.

    CAS  PubMed  Google Scholar 

  • Shibuya, N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ (1987) The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(α2,6)Gal/GalNAc sequence. J Biol Chem 262: 1596–1601.

    CAS  PubMed  Google Scholar 

  • Söderström K (1988) Lectin binding to the human retina. Anat Rec 220: 219–223.

    Article  PubMed  Google Scholar 

  • Spicer S, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: A perspective. J Histochem Cytochem 40: 1–38.

    CAS  PubMed  Google Scholar 

  • Streit WJ, Kreutzberg GW(1987) Lectin binding by resting and reactive microglia. J Neurocytol 16: 149–160.

    Article  Google Scholar 

  • Suzuki H, Franz H, Yamamoto T, Iwasaki Y, Konno H (1988) Identification of the normal microglial population in human and rodent nervous tissue using lectin-histochemistry. Neuropathol Appl Neurobiol 14: 221–227.

    Article  CAS  PubMed  Google Scholar 

  • Takumi K, Uehara F (1991) In vivo lectin-binding of photoreceptors and interphotoreceptor matrix in rat. Jpn J Ophthalmol 35: 16–22.

    CAS  PubMed  Google Scholar 

  • Tien L, Rayborn ME, Hollyfield JG (1992) Characterization of the interphotoreceptor matrix surrounding rod photoreceptors in the human retina. Exp Eye Res 55: 297–306.

    Article  CAS  PubMed  Google Scholar 

  • Turner GA (1992) N-Glycosylation of serum proteins in disease and its investigation using lectins. Clin Chim Acta 208: 149–171.

    Article  CAS  PubMed  Google Scholar 

  • Tyler NK, Burns MS (1991) Comparison of lectin reactivity in the vessel beds of the rat eye. Curr Eye Res 10: 801–810.

    Article  CAS  PubMed  Google Scholar 

  • Uehara F, Ohba N, Sameshima M, Unoki K, Okubo A, Yanagita T, Sugata M, Iwakiri N, Nakagawa S (1994a) Binding of amaranthin in photoreceptors of monkey retina. Jpn J Ophthalmol 38: 360–363.

    CAS  PubMed  Google Scholar 

  • Uehara F, Sameshima M, Unoki K, Okubo A, Yanagita T, Sugata M, Iwakiri N, Ohba N (1994b) Maackia amurensis lectin binding in developing rat retina. Jpn J Ophthalmol 38: 364–367.

    CAS  PubMed  Google Scholar 

  • Uehara F, Yasumura D, LaVail MM (1990) Lectin binding of the interphotoreceptor matrix during retinal development in normal and RCS rats. Curr Eye Res 9: 687–695.

    Article  CAS  PubMed  Google Scholar 

  • Uehara F, Muramatsu T, Sameshima M, Ogata SI, Ohba N (1983) Identification of peanut agglutinin receptors in the monkey retina. Exp Eye Res 37: 303–305.

    Article  CAS  PubMed  Google Scholar 

  • Uehara F, Sameshima M, Muramatsu T, Ohba N (1983) Localization of fluorescence-labeled lectin binding sites on photoreceptor cells of the monkey retina. Exp Eye Res 36: 113–123.

    Article  CAS  PubMed  Google Scholar 

  • Wang WC, Cummings RD (1988) The immobilized leukoagglutinin from the seeds of Maackia amurensis binds with high affinity to complex type Asn-linked oligosaccharides containing terminal sialic acid-linked α-2,3 to penultimate galactose residues. J Biol Chem 263: 4576–4585.

    CAS  PubMed  Google Scholar 

  • Whiteley HE, Scott JR (1990) Lectin binding patterns in developing canine retina. Exp Eye Res 51: 383–391.

    Article  CAS  PubMed  Google Scholar 

  • Wood JG, Besharse JC, Napier-Marshall L (1984) Partial characterization of lectin binding sites of retinal photoreceptor outer segments and interphotoreceptor matrix. J Comp Neurol 228: 299–307.

    Article  CAS  PubMed  Google Scholar 

  • Wood JG, Hart CE, Napier-Marshall L (1986) Microenvironments of photoreceptor and interphotoreceptor matrix glycoconjugates. Histochem J 18: 605–612.

    Article  CAS  PubMed  Google Scholar 

  • 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: 763–766.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, the Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, People's Republic of China

    E.Y.P. Cho, H.L. Choi & Franky L. Chan

Authors
  1. E.Y.P. Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H.L. Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Franky L. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cho, E., Choi, H. & Chan, F.L. Expression pattern of Glycoconjugates in Rat Retina as Analysed by Lectin Histochemistry. Histochem J 34, 589–600 (2003). https://doi.org/10.1023/A:1026032005521

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026032005521

Keywords

Search

Navigation