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Astrocyte invasion and vasculogenesis in the developing ferret retina

  • Published:
Journal of Neurocytology

Abstract

We studied the time course of astrocyte invasion and blood vessel formation in the developing ferret retina using glial fibrillary acidic protein (GFAP)-immunohistochemistry for astrocytes and isolectin B4 histochemistry for blood vessels. As in other mammals, strongly GFAP positive astrocytes invade the ferret retina from the optic nerve. At birth, strongly GFAP positive astrocytes have reached about 22% of the distance between optic disc and outer retinal edge whereas weakly GFAP positive processes already extend to the edge of the retina. At postnatal days P30–P37 about 82% of the distance between optic disc and outer retinal edge and in the adult 88% of this distance is covered with strongly labelled astrocytes. Superficial blood vessels form from the optic disc. They reach up to about 24% of the retinal radius at birth and grow radially across the retina during further development. At P30–P37, the whole retina is covered with superficial blood vessels. The deep vascular layer forms later (around P30) through sprouting from superficial vessels. The radial pattern of astrocyte and vessel growth from the optic disc is not affected by the formation of the area centralis and visual streak.

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References

  • CHAN-LING, T. & STONE, J. (1991) Factors determining the migration of astrocytes into the developing retina: Migration does not depend on intact axons or patent vessels. Journal of Comparative Neurology 303, 375-386.

    Google Scholar 

  • CHAN-LING, T., HALASC, P. & STONE, J. (1990) Development of retinal vasculature in the cat: Processes and mechanisms. Current Eye Research 9, 459-478.

    Google Scholar 

  • CUCCHIARO, J. B. (1991) Early development of the retinal line of decussation in normal and albino ferrets. Journal of Comparative Neurology 312, 193-206.

    Google Scholar 

  • DE SCHAEPDRIJVER, L., SIMOENS, P. & LAUWERS, H. (1995) Development of the retinal circulation in the pig. Anatomy & Embryology 192, 527-536.

    Google Scholar 

  • DISTLER, C. & KIRBY, M. A. (1996) Transience of astrocytes in the newborn macaque monkey retina. European Journal of Neuroscience 8, 847-851.

    Google Scholar 

  • DISTLER, C., KOPATZ, K. & TELKES, I. (2000) Developmental changes in astrocyte density in the macaque perifoveal region. European Journal of Neuroscience 12, 1-11.

    Google Scholar 

  • DISTLER, C., WEIGEL, H. & HOFFMANN, K.-P. (1993) Glia cells of the monkey retina. I. Astrocytes. Journal of Comparative Neurology 333, 134-147.

    Google Scholar 

  • FRUTTIGER, M., CALVER, A. R., KRÑGER, W. H., MUDHAR, H. S., MICHALOVICH, D., TAKAKURA, N., NISHIKAWA, S. I. & RICHARDSON, W. D. (1996) PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17, 1117-1131.

    Google Scholar 

  • GARIANO, R. F., IRUELA-ARISPE, M. L., & HENDRICKSON, A. E. (1994) Vascular development in primate retina: Comparison of laminar plexus formation in monkey and human. Investigative Ophthalmology & Visual Science 35, 3442-3455.

    Google Scholar 

  • GARIANO, R. F., SAGE, E. H., KAPLAN, H. J. & HENDRICKSON, A. E. (1996) Development of astrocytes and their relation to blood vessels in fetal monkey retina. Investigative Ophthalmology and Visual Sciences 37, 2367-2375.

    Google Scholar 

  • GREINER, J. V. & WEIDMAN, T. A. (1981) Histogenesis of the ferret retina. Experimental Eye Research 33, 315-332.

    Google Scholar 

  • GUILLERY, R. W. (1971) An abnormal retinogeniculate projection in the albino ferret (Mustela putorius furo). Brain Research 33, 482-485.

    Google Scholar 

  • HENDERSON, Z. (1985) Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Research 358, 221-228.

    Google Scholar 

  • HENDERSON, Z., FINLAY, B. L. & WIKLER, K. C. (1988) Development of ganglion cell topography in ferret retina. Journal of Neuroscience 8, 1194-1205.

    Google Scholar 

  • HOLLÄNDER, H., MAKAROV, F., DREHER, Z., VAN DRIEL, D., CHAN-LING, T. & STONE, J. (1991) Structure of the macroglia of the retina: Sharing and division of labour between astrocytes and Müller cells. Journal of Comparative Neurology 313, 587-603.

    Google Scholar 

  • HUANG, K. & GUILLERY, R. W. (1985) A demonstration of two distinct geniculocortical projection patterns in albino ferrets. Developmental Brain Research 20, 213-220.

    Google Scholar 

  • HUGHES, A. (1975) A quantitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107-128.

    Google Scholar 

  • HUXLIN, K. R., SEFTON, A. J. & FURBY, J. H. (1992) The origin and development of retinal astrocytes in the mouse. Journal of Neurocytology 21, 530-544.

    Google Scholar 

  • JEFFERY, G. (1997) The albino retina: An abnormality that provides insight into normal retinal development. Trends in Neurosciences 20, 165-169.

    Google Scholar 

  • JEFFERY, G. & KINSELLA, B. (1992) Translaminar deficits in the retinae of albinos. Journal of Comparative Neurology 326, 637-644.

    Google Scholar 

  • JEFFERY, G., DARLING, K. & WHITMORE, A. (1994) Melanin and the regulation of mammalian photoreceptor topography. European Journal of Neuroscience 6, 657-667.

    Google Scholar 

  • JIANG, B., BEZHADIAN, M. A. & CALDWELL, R. B. (1995) Astrocytes modulate retinal vasculogenesis: Effects on endothelial cell differentiation. Glia 15, 1-10.

    Google Scholar 

  • KARSCHIN, A., WÄSSLE, H. & SCHNITZER, J. (1986) Shape and distribution of astrocytes in the cat retina. Investigative Ophthalmology and Visual Sciences 27, 828-831.

    Google Scholar 

  • LING, T. & STONE, J. (1988) The development of astrocytes in the cat retina: Evidence of migration from the optic nerve. Developmental Brain Research 44, 73-85.

    Google Scholar 

  • LING, T., MITROFANIS, J. & STONE, J. (1989) Origin of retinal astrocytes in the rat: Evidence of migration from the optic nerve. Journal of Comparative Neurolology 286, 345-352.

    Google Scholar 

  • MORGAN, J. E., HENDERSON, Z. & THOMPSON, I. D. (1987) Retinal decussation patterns in pigmented and albino ferrets. Neuroscience 20, 519-535.

    Google Scholar 

  • PERRY, V. H. & COWEY, A. (1985) The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Research 25, 1795-1810.

    Google Scholar 

  • QUEVEDO, C., HOFFMANN, K.-P., HUSEMANN, R. & DISTLER, C. (1996) Overrepresentation of the central visual field in the superior colliculus of the pigmented and albino ferret. Visual Neuroscience 13, 627-638.

    Google Scholar 

  • RAMIREZ, J. M., TRIVINO, A., RAMIREZ, SALAZAR, J. J. & GARCIA-SANCHEZ, J. (1994) Immunohistochemical study of human retinal astroglia. Vision Research 34, 1935-1946.

    Google Scholar 

  • RAPAPORT, D. H. & STONE, J. (1984) The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system. Neuroscience 11, 289-301.

    Google Scholar 

  • REESE, B. E., JOHNSON, P. & BAKER, G. E. (1996) Maturational gradients in the retina of the ferret. Journal of Comparative Neurology 375, 252-273.

    Google Scholar 

  • REESE, B. E., THOMPSON, W. F. & PEDUZZI, J. D. (1994) Birthdates of neurons in the retinal ganglion cell layer of the ferret. Journal of Comparative Neurology 341, 464-475.

    Google Scholar 

  • ROBINSON, S. R. & DREHER, Z. (1989) Evidence for three morphological classes of astrocyte in the adult rabbit retina: Functional and developmental implications. Neuroscience Letters 106, 261-268.

    Google Scholar 

  • SCHNITZER, J. (1987) Retinal astrocytes: Their restriction to vascularized parts of the mammalian retina. Neuroscience Letters 78, 29-34.

    Google Scholar 

  • SCHNITZER, J. (1988a) Astrocytes in the guinea pig, horse, and monkey retina: Their occurrence coincides with the presence of blood vessels. Glia 1, 74-89.

    Google Scholar 

  • SCHNITZER, J. (1988b) The development of astrocytes and blood vessels in the postnatal rabbit retina. Journal of Neurocytology 17, 433-449.

    Google Scholar 

  • SCHNITZER, J. & KARSCHIN, A. (1986) The shape and distribution of astrocytes in the retina of the adult rabbit. Cell Tissue Research 246, 91-102.

    Google Scholar 

  • SNODDERLY, D. M., WEINHAUS, R. S. & CHOI, J. C. (1992) Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis). Journal of Neuroscience 12, 1169-1193.

    Google Scholar 

  • STEINBERG, R. H., REID, M. & LACY, P. L. (1973) The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229-248.

    Google Scholar 

  • STONE, J. (1965) A quantitative analysis of the distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 124, 337-352.

    Google Scholar 

  • STONE, J. & DREHER, Z. (1987) Relationship between astrocytes, ganglion cells and vasculature of the retina. Journal of Comparative Neurolology 255, 35-49.

    Google Scholar 

  • STONE, J., ITIN, A., ALON, T., PE'ER, J., GNESSIN, H., CHAN-LING, T. & KESHET, E. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. Journal of Neuroscience 15, 4738-4747.

    Google Scholar 

  • STONE, J. & MASLIM, J. (1997) Mechanics of retinal angiogenesis. Progress in Retinal Eye Research 16, 157-181.

    Google Scholar 

  • TOUT, S., ASHWELL, K. & STONE, J. (1988) The development of astrocytes in the albino rabbit retina and their relationship to retinal vasculature. Neuroscience Letters 90, 241-247.

    Google Scholar 

  • VITEK, D. J., SCHALL, J. D. & LEVENTHAL, A. G. (1985) Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. Journal of Comparative Neurology 241, 1-11.

    Google Scholar 

  • WÄSSLE, H., LEVICK, W. R. & CLELAND, B. G. (1975) The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419-438.

    Google Scholar 

  • WÄSSLE, H., GRÑNERT, U., RÖHRENBECK, J. & BOYCOTT, B. B. (1989) Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643-646.

    Google Scholar 

  • WEBSTER, M. J. & ROWE, M. H. (1991) Disruption of developmental timing in the albino rat retina. Journal of Comparative Neurology 307, 460-474.

    Google Scholar 

  • WOLTER, J. R. (1955) The cells of Remak and the astroglia of the normal human retina. Archives of Ophthalmology 53, 832-838.

    Google Scholar 

  • ZHANG, H. Y. & HOFFMANN, K.-P. (1993) Retinal projections to the pretectum, accessory optic system and superior colliculus in pigmented and albino ferrets. European Journal of Neurosciences 5, 486-500.

    Google Scholar 

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Kopatz, K., Distler, C. Astrocyte invasion and vasculogenesis in the developing ferret retina. J Neurocytol 29, 157–172 (2000). https://doi.org/10.1023/A:1026594721760

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