Concentration of astrocytic filaments at the retinal optic nerve junction is coincident with the absence of intra-retinal myelination: comparative and developmental evidence
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The structure of the lamina cribrosa (LC) and astrocytic density were examined in various species with and without intra-retinal myelination. Sections of optic nerve from various species were stained with Milligan's trichrome or antibodies to glial fibrillary acidic protein, myelin basic protein (MBP) and antibody O4. Marmoset, flying fox, cat, and sheep, which lack intraretinal myelination, were shown to possess a well-developed LC as well as a marked concentration of astrocytic filaments distal to the LC. Rat and mouse, which lack intraretinal myelination, lacked a well-developed LC but exhibited a marked concentration of astrocytic filaments in this region. Rabbit and chicken, which exhibit intraretinal myelination, lacked both a well-developed LC and a concentration of astrocytes at the retinal optic nerve junction (ROJ). A marked concentration of astrocytes at the ROJ of human fetuses was also apparent at 13 weeks of gestation, prior to myelination of the optic nerve; in contrast, the LC was not fully developed even at birth. This concentration of astrocytes was located distal to O4 and MBP immunoreactivity in human optic nerve, and coincided with the site of initial myelination of ganglion cell axons in marmoset and rat. Myelination proceeded from the chiasm towards the retinal end of the human optic nerve. Moreover, the outer limit of oligodendrocyte precursor cells (OPC) migration into the rabbit retina was restricted by the outer limit of astrocyte spread. These observations indicate that a concentration of astrocytic filaments at the ROJ is coincident with the absence of intraretinal myelination. Differential expression of tenascin-C by astrocytes at the ROJ appears to contribute to the molecular barrier to OPC migration (see Bartsch et al., 1994), while expression of the homedomain protein Vax 1 by glial cells at the optic nerve head appears to inhibit migration of retinal pigment epithelial cells into the optic nerve (see Bertuzzi et al., 1999). These observations combined with our present comparative and developmental data lead us to suggest that the astrocytes at the ROJ serve to regulate cellular traffic into and out of the retina.
- ANDERSON, D. R. & HENDRICKSON, A. (1974) Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve. Investigative Ophthalmology and Visual Science 13, 771-783.
- ARMSTRONG, R. C., DORN, H. O. H., KUFTA, C. V., FRIEDMAN, E. & DUBOIS-DALCQ, M. E. (1992) Preoligodendrocytes from adult human CNS. Journal of Neuroscience 12, 1538-1547.
- BARTSCH, S., BARTSCH, U., DORRIES, U., FAISSNER, A., WELLER, A., EKBLOM, P. & SCHACHNER, M. (1992) Expression of tenascin in the developing and adult cerebellar cortex. Journal of Neuroscience 12, 736-749.
- BARTSCH, U., FAISSNER, A., TROTTER, J., DÖRRIES, U., BARTSCH, S., MOHAJERI, H. & SCHACHNER, M. (1994) Tenascin demarcates the boundary between the myelinated and non-myelinated part of retinal ganglion cell axons in the developing and adult mouse. Journal of Neuroscience 14, 4756-4768.
- BARTSCH, U., KIRCHHOFF, F. & SCHACHNER, M. (1989) Immunohistological localization of the adhesion molecules L1, N-CAM, and MAG in the developing and adult optic nerve of mice. Journal of Comparative Neurology 284, 451-462.
- BARTSCH, U. (1996) The extracellular matrix molecule tenascin-C: expression in vivo and functional characterization in vitro. Progress in Neurobiology 49, 145-168.
- BERLINER, M. L. (1931) Cytological studies on the retina. I. Normal coexistence of oligodendroglia and myelinated nerve fibres. Archives of Ophthalmology 6, 740-751.
- BERTUZZI, S., HINDGES, R., MUI, S. H., O'LEARY, D. D. M. & LEMKE, G. (1999) The homeodomain protein Vax 1 is required for axon guidance and major tract formation in the developing forebrain Genes and Development. 13, 3092-105.
- BLUNT, M. J., WENDELL-SMITH, C. P. & BALDWIN, F. (1965). Glia-nerve fibre relationships in mammalian optic nerve. Journal of Anatomy (London) 99, 1-11.
- COLELLO, R. J., DEVEY, L. R., IMPERATO, E. & POTT, U. (1995) The chronology of oligodendrocyte differentiation in the rat optic nerve: evidence for a signaling step initiating myelination in the CNS. Journal of Neuroscience 15, 7665-7672.
- DUKE-ELDER, S. & COOK, C. (1963) System of Ophthalmology: Normal and Abnormal Development. I. Embryology. p. 119 St. Louis: Mosby.
- ELKINGTON, A. R., INMAN, C. B. E., STEWART, P. V. and WELLER, R. O. (1990). The structure of the lamina cribrosa of the human eye: an immunocytochemical and electron microscopical study. Eye 4, 42-57.
- FFRENCH-CONSTANT, C., MILLER, R. H., BURNE, J. F., RAFF, M. C. (1988) Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve. Journal of Neurocytology 17, 13-25.
- FITZGIBBON, T. & NESTOROVSKI, Z. (1997) Morphological consequences of myelination in the human retina. Experimental Eye Research 65, 809-819.
- FLAGE, T. (1977) Permeability properties of the tissues in the optic nerve head region in the rabbit and the monkey. Acta Ophthalmologica 55, 652-664.
- FULTON, B. P., BURNE, J. F. & RAFF, M. C. (1992). Visualization of O-2A progenitor cells in developing and adult rat optic nerve by quisqualatestimulated cobalt uptake. Journal of Neuroscience 12, 4816-4833.
- GRUMET, M., HOFFMAN, S., CROSSIN, K. L. & EDELMAN, G. M. (1985) Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proceedings of the National Academy of Sciences USA 82, 8075-8079.
- HILDEBRAND, C., REMAHL, S. & WAXMAN, S. G. (1985) Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations. Journal of Neurocytology 14, 597-617.
- HU, P., POLLARD, J., HUNT, N., TAYLOR, J. & CHANLING, T. (1998) Microvascular and cellular responses in the optic nerve of rats with acute experimental allergic encephalomyelitis (EAE). Brain Pathology 8, 475-486.
- HUANG, P. P., ALLIQUANT, B., CARMEL, P. W., FRIEDMAN, E. D. (1991) Myelination of the rat retina by transplantation of oligodendrocytes into 4-day-old hosts. Experimental Neurology 113, 291-300.
- KIERNAN, B. W, GOTZ, B., FAISSNER, A. & FFRENCH-CONSTANT, C. (1996) Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesiondependent and adhesion-independent mechanisms. Molecular and Cellular Neuroscience 7, 322-335.
- KISTLER, H. B. & LA VAIL, J. H. (1981) Penetration of horseradish peroxidase into the optic nerve after vitreal or vascular injections in the developing chick. Investigative Ophthalmology and Visual Science 20, 705-716.
- 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.
- LAENG, P., MOLTHAGEN, M., YU, E. G., & BARTSCH, U. (1996). Transplantation of oligodendrocyte progenitor cells into the rat retina: extensive myelination of retinal ganglion cell axons. Glia 18, 200-210.
- MA, N., HUNT, N. H., MADIGAN, M. C. & CHAN-LING, T. (1996) Correlation between enhanced vascular permeability, up-regulation of cellular adhesion molecules and monocyte adhesion to the endothelium in the retina during the development of fatal murine cerebral malaria. American Journal of Pathology 149, 1745-1762.
- MAGOON, E. H. & ROBB, R. M. (1981) Development of myelin in human optic nerve and tract. A light and electron microscopic study. Archives of Ophthalmology 99, 655-659.
- MILLIGAN, M. (1946) Trichrome stain for formalin-fixed tissue. American Journal of Clinical Pathology 10, 184-185.
- MITROVIC, N. & SCHACHNER, M. (1995) Detection of tenascin-C in the nervous system of the tenascin-C mutant mouse. Journal of Neuroscience Research 42, 710-717.
- MORCOS, Y. & CHAN-LING, T. (1997) Identification of oligodendrocyte precursors in the myelinated streak of the adult rabbit retina in vivo. Glia 21, 163-182.
- MORCOS, Y., SHOREY, C. D. & CHAN-LING, T. (1999) Contribution of O4+ oligodendrocyte precursors and astrocytes to the glial ensheathment of vessels in the rabbit myelinated streak. Glia 27, 1-14.
- MORRISON, J. C., JERDAN, J. A., DORMAN, M. E. & QUIGLEY H. A. (1989) Structural proteins of the neonatal and adult lamina cribrosa. Archives of Ophthalmology 107, 1220-1224.
- NAKAZAWA, T., TACHI, S., AIKAWA, E. & IHUMA, M. (1993). Formation of the myelinated nerve fibre layer in the chicken retina. Glia 8, 114-121.
- NOBLE, M., WREN, D. & WOLSWIJK, G. (1992) The O-2A (adult) progenitor cell: a glial stem cell of the adult central nervous system. Seminars in Cell Biology 3, 413-422.
- ONO, K., TSUMORI, T., KISHI, T., YOKOTA, S. & YASUI, Y. (1998) Developmental appearance of oligodendrocytes in the embryonic chick retina. Journal of Comparative Neurology 398, 309-322.
- OXLUND, H. (1986) Relationships between the biomechanical properties, composition and molecular structure of connective tissues. Connective Tissue Research 15, 65-72.
- PERRY, V. H. & LUND, R. D. (1990) Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons. Journal of Neurocytology 19, 265-272.
- POTTER, E. L. & GRAIG, J. M. (1975) Pathology of the Fetus and the Infant. Chicago: Yearbook Medical Publishers, pp 29-37.
- PRINGLE, N. P., MUDHAR, H. S., COLLARINI, E. J. & RICHARDSON, W. D. (1992). PDGF receptors in the rat CNS: During late neurogenesis, PDGF ?-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115, 535-551.
- QUIGLEY, H. A., ADDICKS, E. M., GREEN, W. R. & MAUMENEE, A. E. (1981) Optic nerve damage in human glaucoma. II. The site of injury and susceptibility to damage. Archives of Ophthalmology 99, 635-649.
- SAGA, Y., YAGI, T., IKAWA, Y., SAKAKURA, T. & AIZAWA, S. (1992) Mice develop normally without tenascin. Genes and Development 6, 1821-1831.
- SATTLER, C. H. (1915). Ñber die Markscheidenentwicklung im Tractus opticus: Chiasma und Nervus opticus. Albrecht Von Graefes Archiv Fur Ophthalmologie 90, 271-298.
- SHI, J., MARINOVICH, A. & BARRES, B. A. (1998) Purification and characterization of adult oligodendrocyte precursors fromthe rat optic nerve. Journal of Neuroscience 18, 4627-4636.
- SKOFF, R., KNAPP, P. E. & BARTLETT, W. P. (1986) Astrocyte diversity in the optic nerve: a cytoarchitectural study. In Astrocytes, Vol. 1. (edited by FEDOROFF, S. & VERNADAKIS, A.) New York: Academic Press. pp 269-291.
- SMALL, R. K., RIDDLE, P. & NOBLE, M. (1987) Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 328, 155-157.
- SOMMER, I. & SCHACHNER, M. (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Developmental Biology 83, 311-327.
- TANSLEY, K. (1956) Comparison of the lamina cribrosa in mammalian species with good and with indifferent vision. British Journal of Ophthalmology 40, 178-182.
- TSO, M. O. M., SHIH, C. Y. & MCLEAN, M. I. W. (1975) Is there a blood-brain barrier at the optic nerve head? Archives of Ophthalmology 93, 815-825.
- TSUKAMOTO, T., KUSAKABE, M. & SAGA, Y. (1991) In situ hybridization with non-radioactive digoxigenin-11-UTP-labeled cRNA probes: localization of developmentally regulated mouse tenascin mRNAs. The International Journal of Developmental Biology 35, 25-32.
- WOLBURG, H. & BÄUERLE, C. (1993) Astrocytes in the lamina cribrosa of the rat optic nerve: Are their morphological peculiarities involved in an altered blood-brain barrier? Journal für Hirnforschung 34, 445-459.
- WOLSWIJK, G. (1998) Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. Journal of Neuroscience 18, 601-609.
- Concentration of astrocytic filaments at the retinal optic nerve junction is coincident with the absence of intra-retinal myelination: comparative and developmental evidence
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