Abstract
Based on the idea of differentiation-related changes in the glycosylation pattern of neurons, the expression of two cell surface oligosaccharide epitopes, N-acetyl-lactosamine (NALA), and its sulpho-glucuronyl derivative (HNK-1), was studied, by immunohistochemistry and Western blot experiments, in the developing chick retina beginning on day 2 of incubation (E2) until day 18 post-hatching. NALA was detectable on neuroepithelial cells as soon as the primary optic vesicles formed, and this pattern continued until E3. During subsequent retinal development NALA expression became progressively restricted in concert with the appearance of postmitotic neurons as revealed by neurite outgrowth, and with the formation of synaptic contacts until it disappeared at the end of the incubation period. The pattern of NALA expression was the inverse of HNK-1 which was detected for the first time at E3 on postmitotic ganglion cells accumulating at the vitreal surface. The number of HNK-1+ cells steadily increased until around E10, when the entire neural epithelium was labelled. Synchronously to synaptogenesis, most neurons lost their HNK-1 immunoreactivity. At the time of hatching the adult-like pattern was found, characterised by subpopulations of labelled horizontal, bipolar, amacrine, and ganglion cells. Immunoblot experiments demonstrated transient NALA glycosylation of protein bands, partially identical in their apparent molecular weight to those proteins with HNK-1 glycosylation. The observed temporospatial changes in the glycosylation patterns of distinct proteins during retinal development suggest NALA as a suitable marker for neuronal proliferation, and HNK-1 for differentiation and establishment of final synaptic configuration.
Similar content being viewed by others
References cited
Andressen C, Mai JK (1997a) Lactoseries carbohydrate epitopes in the vertebrate retina. Histochem J 29: 1-9.
Andressen C, Mai JK (1997b) Distribution of CD15 in the vertebrate retina. Vis Neurosci 14: 253-262.
Andressen C, Moertter K, Mai JK (1996) Spatiotemporal expression of CD15 in the developing chick retina. Dev Brain Res 95: 263-271.
Andressen C, Arnhold S, Mai JK (1998) Differential expression of lactoseries carbohydrate epitopes HNK-1, CD15, andNALA by olfactory receptor neurons in the developing chick. Anat Embryol 197: 209-215.
Ball ED (1995) Introduction: Workshop Summary of the CD15 Monoclonal Antibody Panel from the Fifth International Workshop on Leukocyte Antigens. Eur J Morphol 33: 95-100.
Breen KC, Coughlan CM, Hayes FD (1998) The role of glycoproteins in neural development function, and disease. Mol Neurobiol 16: 163-220.
Coulombre AS (1955) Correlations of structural and biochemical changes in the developing retina of the chick. Am J Anat 96: 153-184.
Daniels MP, Vogel Z (1980) Localization of alpha bungarotoxin binding sites in synapses of the developing chick retina. Brain Res 201: 45-56.
Devries T, Van Den Eijnden DH (1992) Occurence and specifities of alpha3-fucosyltransferases. Histochem J 24: 761-770.
Dodd J, Jessel TM (1985) Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal chord. J Neurosci 5: 3278-3292.
Dodd J, Jessel TM (1986) Cell surface glycoconjugates and carbohydrate binding proteins: possible recognition signals in sensory neurone development. J Exp Biol 124: 225-238.
Feizi T (1985) Demonstration by monoclonal antibodies that carbohydrate structures of glycoproteins and glycolipids are oncodevelopmental antigens. Nature 314: 53-57.
Fenderson BA, Eddy EM, Hakomori S (1988) The blood group Iantigen defined by monoclonal antibody C6 is a marker of early mesoderm during murine embryogenesis. Differentiation 38: 124-133.
Fujita S, Horii S (1963) Analysis of cytogenesis in the chick retina by tritiated thymidine autoradiography. Arch Histol Jap 23: 295-366.
Hakomori S (1992) LeX and related structures as adhesion molecules. Histochem J 24: 771-776.
Hakomori S, Kannagi R (1983) Glycosphingolipids as tumor-associated and differentiation markers. J Natl Cancer Inst 71: 231-251.
Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morph 88: 49-92.
Hughes WF, Lavelle A (1974) On the synaptogenetic sequence in the chick retina. Anat Rec 179: 297-301.
Kahn AJ (1974) An autoradiographic analysis of the time of appearance of neurons in the developing chick neural retina. Dev Biol 38: 30-40.
Kruse J, Mailhammer R, Wernecke H, Faissner A, Sommer I, Goridis I, Schachner M (1984) Neuronal cell adhesion molecules and myelin associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibody L2 and HNK-1. Nature 311: 153-155.
Kruse J, Keilhauer G, Faissner A, Timpl R, Schachner M (1985) The J1 glycoprotein-a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature 316: 146-148.
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 227: 680-685.
Lemmon V, Farr KL, Lagenaur C (1989) L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2: 1597-1603.
Mai JK, Marani E, Hakomori S (1992) Guest editorial. Histochem J 24: 759-760.
Mai JK, Bartsch D, Marani E (1995) CD15 and HNK-1 reveal cerebellar compartments with a complex overlap. Eur J Morphol 33: 101-107.
Mai JK, Andressen C, Ashwell K (1998) Demarcation of prosencephalic regions by CD15 positive radial glia. Eur J Neurosci 10: 746-751.
Marani E, Tetteroo PAT (1983) Alongitudinal band pattern for the monoclonal human granulocyte antibody B4,3 in the cerebellar external granular layer of the immature rabbit. Histochemistry 78: 157-161.
Marani E, Tetteroo PAT, Van Der Vecken J (1983) The ultrastructure localization of the monoclonal human granulocyte antibody B4,3 in cell suspension of the immature rabbit cerebellum. Cell Biol Int Rep 7: 763-769.
Marani E, Van Der Vecken JGPM, Lakke EAJF (1995) Simultaneous demonstration of CD15 and alkaline phosphatase activity in cryostat sections of rat fetuses. A detailed technical discription for the developing brain. Eur J Morphol 33: 137-147.
McGarry RC, Helfand SL, Quarles RH, Roder JC (1983) Recognition of myelin associated glycoprotein by the monoclonal antibody HNK-1. Nature 306: 367-378.
Metcalfe WK, Myers PZ, Trevarrow B, Bass MB (1990) Primary neurons that express the L2/HNK-1 carbohydrate during early development of the zebrafish. Development 110: 491-504.
Prada C, Puga J, Perez Mendez L, Lopez R, Ramirez G (1991) Spatial and temporal patterns of neurogenesis in the chick embryo retina. Eur J Neurosci 3: 559-569.
Reifenberger G, Mai JK, Krajewski S, Wechsler WS (1987) Distribution of anti-Leu-7, anti-Leu-11a and anti-Leu-M-1 immunoreactivity in the brain of the adult rat. Cell Tiss Res 248: 305-313.
Rutishauser U, Acheson A, Hall AK, Mann DM, Sunshine J (1988) The neural cell adhesion molecules (NCAM) as a regulator of cell-cell interaction. Science 240: 53-57.
Schachner M (1989) Families of Neural Adhesion Molecules. Carbohydrate Recognition in Cellular Function. Chichester: John Wiley & Sons, pp. 156-172.
Solter D, Knowles BB (1978) Monoclonal antibody defining a stage specific mouse embryonic antigen (SSEA-1). Proc Natl Acad Sci USA 75: 5565-5569.
Spence SG, Robson JA (1989) An autoradiographic analysis of neurogenesis in the chick retina in vitro and in vivo. Neuroscience 32: 801-812.
Springer TA, Lasky LA (1991) Sticky sugars for selectins. Nature 349: 196-197.
Tucker GC, Aoyama H, Lipinski M, Tursz T, Thiery JP (1984) Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ 14: 223-230.
Tucker GC, Delarue M, Zada S, Boucaut JC, Thiery JP (1988) Expression of the HNK-1/NC-1 epitope in early vertebrate neurogenesis. Cell Tissue Res 251: 457-465.
Uusitalo M, Kivelä T (1994) Differential distribution of the HNK-1 carbohydrate epitope in the vertebrate retina. Curr Eye Res 13: 697-704.
Uusitalo M, Kivelä T (1997) The HNK-1 epitope in the pseudophakic and aphakic eye and secondary cataract. Acta Ophthalmol Scand 75: 516-519.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Andressen, C., Arnhold, S., Ashwell, K. et al. Stage Specific Glycosylation Pattern for Lactoseries Carbohydrates in the Developing Chick Retina. Histochem J 31, 331–338 (1999). https://doi.org/10.1023/A:1003722102996
Issue Date:
DOI: https://doi.org/10.1023/A:1003722102996