Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T14:54:38.989Z Has data issue: false hasContentIssue false
  • English
  • Français

Gradients of cone differentiation and FGF expression during development of the foveal depression in macaque retina

Published online by Cambridge University Press:  06 October 2005

ELISA E. CORNISH ,
MICHELE C. MADIGAN ,
RICCARDO NATOLI ,
ANGELA HALES ,
ANITA E. HENDRICKSON  and
JAN M. PROVIS
ELISA E. CORNISH
Affiliation:
Department of Ophthalmology and Save Sight Institute, University of Sydney, NSW 2006, Australia
MICHELE C. MADIGAN
Affiliation:
Department of Ophthalmology and Save Sight Institute, University of Sydney, NSW 2006, Australia
RICCARDO NATOLI
Affiliation:
Research School of Biological Sciences, Bldg. 46, Biology Place, The Australian National University, Canberra, ACT 0200, Australia
ANGELA HALES
Affiliation:
Department of Ophthalmology and Save Sight Institute, University of Sydney, NSW 2006, Australia
ANITA E. HENDRICKSON
Affiliation:
Department of Biological Structure, University of Washington, Seattle
JAN M. PROVIS
Affiliation:
Research School of Biological Sciences, Bldg. 46, Biology Place, The Australian National University, Canberra, ACT 0200, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Cones in the foveola of adult primate retina are narrower and more elongated than cones on the foveal rim, which in turn, are narrower and more elongated than those located more eccentric. This gradient of cone morphology is directly correlated with cone density and acuity. Here we investigate the hypothesis that fibroblast growth factor (FGF) signaling mediates the morphological differentiation of foveal cones—in particular, the mechanism regulating the elongation of foveal cones. We used immunoreactivity to FGF receptor (R) 4, and quantitative analysis to study cone elongation on the horizontal meridian of macaque retinae, aged between foetal day (Fd) 95 and 2.5 years postnatal (P 2.5y). We also used in situ hybridization and immunohistochemistry to investigate the expression patterns of FGF2 and FGFR1–4 at the developing fovea, and three other sample locations on the horizontal meridian. Labeled RNA was detected using the fluorescent marker “Fast Red” (Roche) and levels of expression in cone inner segments and in the ganglion cell layer (GCL) were compared using confocal microscopy, optical densitometry, and tested for statistical significance. Our results show that morphological differentiation of cones begins near the optic disc around Fd 95, progressing toward the developing fovea up until birth, approximately. Levels of FGF2 and FGFR4 mRNAs expression are low in foveal cones, compared with cones closer to the optic disc, during this period. There is no similar gradient of FGF2 mRNA expression in the ganglion cell layer of the same sections. Maturation of foveal cones is delayed until the postnatal period. The results suggest that a wave of cone differentiation spreads from the disc region toward the developing fovea during the second half of gestation in the macaque. A gradient of expression of FGFR4 and FGF2 associated with the wave of differentiation suggests that FGF signalling mediates cone narrowing and elongation.

Keywords

Fovea centralisCone morphogenesisFibroblast growth factorsRetinaPrimate
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 447 - 459
Copyright
2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abramov, I., Gordon, J., Hendrickson, A., Hainline, L., Dobson, V., & LaBossiere, E. (1982). The retina of the newborn human infant. Science 217, 265–7.Google Scholar
Bach, L. & Seefelder, R. (1911, 1912, 1914). Entwicklungsgeschichte des menschlichen auges. Leipzig, W. Engelmann.
Baudouin, C., Fredj-Reygrobellet, D., Caruelle, J.P., Barritault, D., Gastaud, P., & Lapalus, P. (1990). Acidic fibroblast growth factor distribution in normal human eye and possible implications in ocular pathogenesis. Ophthalmic Research 22, 73–81.Google Scholar
Bumsted, K. & Hendrickson, A. (1999). Distribution and development of short-wavelength cones differ between Macaca monkey and human fovea. Journal of Comparative Histology 403, 502–516.Google Scholar
Candy, T.R., Crowell, J.A., & Banks M.S. (1998). Optical, receptoral, and retinal constraints on foveal and peripheral vision in the human neonate. Vision Research 38, 3857–3870.Google Scholar
Caruelle, D., Groux-Muscatelli, B., Gaudric, A., Sestier, C., Coscas, G., Caruelle, J.P., & Baritault, D. (1989). Immunological study of acidic fibroblast growth factor (aFGF) distribution in the eye. Journal of Cellular Biochemistry 39, 117–128.Google Scholar
Colvin, J.S., Feldman, B., Nadeau, J.H., Goldfarb, M., & Ornitz, D.M. (1999). Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Developmental Dynamics 216, 72–88.Google Scholar
Connolly, S.E., Hjelmeland, L.M., & LaVail, M.M. (1992). Immunohistochemcial localization of basic fibroblast growth factor in mature and developing retinas of normal and RCS rats. Current Eye Research 11, 1006–1017.Google Scholar
Cornish, E.E., Natoli, R.C., Hendrickson, A., & Provis, J.M. (2004). Differential distribution of fibroblast growth factor receptors (FGFRs) on foveal cones: FGFR-4 is an early marker of cone photoreceptors. Molecular Vision 10, 1–14.Google Scholar
Crooks, J., Okada, M., & Hendrickson, A.E. (1995). Quantitative analysis of synaptogenesis in the inner plexiform layer of macaque monkey fovea. Journal of Comparative Neurology 360, 349–362.Google Scholar
de Iongh, R.U., Lovicu, F.J., Hannekan, A., Baird, A., & McAvoy, J.W. (1996). FGF-receptor 1 (flg) expression is correlated with fibre differentiation during rat lens morphogenesis and growth. Developmental Dynamics 206, 412–426.Google Scholar
de Iongh, R.U., Lovicu, F.J., Chamberlain, C.G., & McAvoy J.W. (1997). Differential expression of fibroblast growth factor receptors during rat lens morphogenesis and growth. Investigative Ophthalmology and Visual Science 38, 1688–1699.Google Scholar
Diaz-Araya, C.M. & Provis, J.M. (1992). Evidence of photoreceptor migration during early foveal development: A quantitative analysis of human fetal retinae. Visual Neuroscience 8, 505–514.Google Scholar
Dobson, V. & Teller, D.Y. (1978). Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research 18, 1469–1483.Google Scholar
Engerman, R.L. (1976). Development of the macular circulation. Investigative Ophthalmology 15, 835–840.Google Scholar
Gao, H. & Hollyfield, J.G. (1995). Basic fibroblast growth factor in retinal development: Differential levels of bFGF expression and content in normal and retinal degeneration (rd) mutant mice. Developmental Biology 169, 168–184.Google Scholar
Gariano, R.F., Iruela, A.M., & Hendrickson, A.E. (1994). Vascular development in primate retina: 1. Comparison of laminar plexus formation in monkey and human. Investigative Ophthalmology and Visual Science 35, 3442–3455.Google Scholar
Georges, P., Madigan, M.C., & Provis, J.M. (1999). Apoptosis during development of the human retina: Relationship to foveal development and retinal synaptogenesis. Journal of Comparative Neurology 413, 198–208.Google Scholar
Hageman, G.S., Kirchoff-Rempe, M.A., Lewis, G.P., Fisher, S.K., & Anderson, D.H. (1991). Sequestration of basic fibroblast growth factor in the primate interphotoreceptor matrix. Proceedings of the National Academy of Sciences of the U.S.A. 88, 6706–6710.Google Scholar
Hendrickson, A. (1992). A morphological comparison of foveal development in man and monkey. Eye 6, 136–144.Google Scholar
Hendrickson, A. (1994). Primate foveal development: A microcosm of current questions in neurobiology. Investigative Ophthalmology and Visual Science 35, 3129–3133.Google Scholar
Hendrickson, A. & Drucker, D. (1992). The development of parafoveal and mid-peripheral human retina. Behavioural Brain Research 49, 21–31.Google Scholar
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746–756.Google Scholar
Hendrickson, A.E. (1988). Development of the primate retina. In Handbook of Growth and Developmental Biology, Vol. 1B, ed. Timiras, P.S., pp. 165–178. Boca Raton, Florida: CRC Press.
Hendrickson, A.E. (1996). Synaptic development in macaque monkey retina and its implications for other developmental sequences. Perspectives on Developmental Neurobiology 3, 195–201.Google Scholar
Hendrickson, A.E. & Yuodelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603–612.Google Scholar
Kay, E., Park, S., Ko, M., & Lee, S. (1998). Fibroblast growth factor 2 uses PLC-gamma1 for cell proliferation and PI3-kinase for alteration of cell shape and cell proliferation in corneal endothelial cells. Molecular Vision 4, 22.Google Scholar
Kirby, M.A. & Steineke, T.C. (1996). Morphogenesis of retinal ganglion cells: A model of dendritic, mosaic, and foveal development. Perspectives on Developmental Neurobiology 3, 177–194.Google Scholar
Kitaoka, T., Aotaki-Keen, A.E., & Hjelmeland, L.M. (1994). Distribution of FGF-5 in the rhesus macaque retina. Investigative Ophthalmology and Visual Science 35, 3189–3198.Google Scholar
Li, Z.Y., Chang, J.H., & Milam, A.H. (1997). A gradient of basic fibroblast growth factor in rod photoreceptors in the normal human retina. Visual Neuroscience 14, 671–679.Google Scholar
Linberg, K.A. & Fisher, S.K. (1990). A burst of differentiation in the outer posterior retina of the eleven-week human fetus: An ultrastructural study. Visual Neuroscience 5, 43–60.Google Scholar
Lovicu, F.J. & McAvoy, J.W. (1993). Localization of acidic fibroblast growth factor, basic fibroblast growth factor and heparan sulphate proteoglycans in rat lens: Implications for lens polarity and growth patterns. Investigative Ophthalmology and Visual Science 34, 3355–3365.Google Scholar
Mann, I. (1964). The Development of the Human Eye. (First published 1928). New York: Grune and Stratton.
McAvoy, J.W., Chamberlain, C.G., de Iongh, R.U., & Richardson, N.A. (1991). The role of fibroblast growth factors (FGF) in eye lens development. Annals of the New York Academy of Sciences 638, 256–274.Google Scholar
Mervin, K., Valter, K., Maslim, J., Lewis, G., Fisher, S., & Stone, J. (1999). Limiting photoreceptor death and deconstruction during experimental retinal detachment: The value of oxygen supplementation. American Journal of Ophthalmology 128, 155–164.Google Scholar
Noji, S., Matsuo, T., Koyama, E., Yamaai, T., Nohno, T., Matsuo, N., & Taniguchi, S. (1990). Expression pattern of acidic and basic fibroblast growth factor in adult rat eyes. Biochemical and Biophysical Research Communications 168, 343–349.Google Scholar
Okada, M., Erickson, A., & Hendrickson, A. (1994). Light and electron microscopic analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for the synaptic vesicle protein, SV2. Journal of Comparative Neurology 339, 535–58.Google Scholar
Ornitz, D.M., Xu, J., Colvin, J.S., McEwen, D.G., MacArthur, C.A., Coulier, F., Gao, G., & Goldfarb, M. (1996). Receptor Specificity of the Fibroblast Growth factor family. Journal of Biological Chemistry 271, 15292–15297.Google Scholar
Packer, O., Hendrickson, A.E., & Curcio, C.A. (1990). Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina. Journal of Comparative Neurology 298, 472–493.Google Scholar
Provis, J.M. (2001). Development of the primate retinal vasculature. Progress in Retinal and Eye Research 20, 799–821.Google Scholar
Provis, J.M., Billson, F.A.B., & Russell, P. (1983). Ganglion cell topography in human fetal retinae. Investigative Ophthalmology and Visual Science 24, 1316–1320.Google Scholar
Provis, J.M., Diaz, C.M., & Dreher, B. (1998). Ontogeny of the primate fovea: A central issue in retinal development. Progress in Neurobiology 54, 549–580.Google Scholar
Provis, J.M. & Penfold, P.L. (1988). Cell death and the elimination of retinal axons during development. Progress in Neurobiology 31, 331–347.Google Scholar
Provis, J.M., Sandercoe, T., & Hendrickson, A.E. (2000). Astrocytes and blood vessels define the foveal rim during primate retinal development. Investigative Ophthalmology and Visual Science 41, 2827–2836.Google Scholar
Rapaport, D.H. & Stone, J. (1982). The site of commencement of maturation in mammalian retina: Observations in the cat. Developmental Brain Research 5, 273–279.Google Scholar
Springer, A. & Hendrickson, A. (2004a). Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation. Visual Neuroscience 21, 53–62.Google Scholar
Springer, A. & Hendrickson, A. (2004b). Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retinal and pars plana growth. Visual Neuroscience 21, 775–790.Google Scholar
Springer, A. & Hendrickson, A. (2005). Development of the primate area of high acuity. 3. temproal relationships between pit formation, retinal elongation and cone packing. Visual Neuroscience 22, 171–185.Google Scholar
Vogel-Hopker, A., Momose, T., Rohrer, H., Yasuda, K., Ishihara, L., & Rapaport, D.H. (2000). Multiple functions of fibroblast growth factor-8 (FGF-8) in chick eye development. Mechanisms of Development 94, 25–36.Google Scholar
Wässle, H., Grünert, U., Röhrenbeck, J., & Boycott, B.B. (1990). Retinal ganglion cell density and the cortical magnification factor in the primate. Vision Research 30, 1897–1911.Google Scholar
Williams, R.A. & Booth, R.G. (1981). Development of optical quality in the infant monkey (Macaca nemestrina) eye. Investigative Ophthalmology and Visual Science 21, 728–36.Google Scholar
Xiao, M. & Hendrickson, A. (2000). Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. Journal of Comparative Neurology 425, 545–559.Google Scholar
Xie, M.H., Holcomb, I., Deuel, B., Dowd, P., Huang, A., Vagts, A., Foster, J., Liang, J., Brush, J., Gu, Q., Hillan, K., Goddard, A., & Gurney, A.L. (1999). FGF-19, a novel fibroblast growth factor with unique specificity for FGFR4. Cytokine 11, 729–735Google Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.Google Scholar