Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T17:57:00.430Z Has data issue: false hasContentIssue false
  • English
  • Français

Appearance of cGMP-phosphodiesterase immunoreactivity parallels the morphological differentiation of photoreceptor outer segments in the rat retina

Published online by Cambridge University Press:  02 June 2009

Laura Colombaioni  and
Enrica Strettoi
Laura Colombaioni
Affiliation:
Istituto di Neurofisiologia del CNR, 56127 Pisa, Italy
Enrica Strettoi
Affiliation:
Istituto di Neurofisiologia del CNR, 56127 Pisa, Italy
Get access Rights & Permissions [Opens in a new window]

Abstract

We have investigated by immunofluorescence the appearance of immunoreactive guanosine 3′-5′ cyclic monophosphate phosphodiesterase (cGMP-PDE) during the postnatal development of the retina of the pigmented rat. We show that a sudden increase in immunoreactivity takes place during postnatal day five (P5), when rod outer segments begin to form; immunoreactivity develops rapidly in the following days. Labeling is restricted to the developing photoreceptor outer segments, sparing other retinal cells, as confirmed by electron microscopy immunocytochemistry. In addition, cGMP-PDE immunoreactivity follows a center-to-periphery gradient paralleling photoreceptor differentiation. It appears that cGMP-PDE is expressed when the photoreceptor subcellular compartments are already formed, and represents a specific marker of late photoreceptor differentiation. The appearance of cGMP-PDE during development is temporally correlated with the appearance of other proteins of the phototransduction machinery.

Keywords

PhototransductionRetinal developmentImmunocytochemistryPhosphodiesterase
Type
Articles
Information
Visual Neuroscience , Volume 10 , Issue 3 , May 1993 , pp. 395 - 402
Copyright
Copyright © Cambridge University Press 1993

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

Ahmad, I., Redmond, L.J. & Barnstable, C.J. (1990). Developmental and tissue-specific expression of the rod photoreceptor cGMP-gated ion channel gene. Biochemical and Biophysical Research Communications 173, 463–470.CrossRefGoogle ScholarPubMed
Balkema, G.W. & Drager, U.C. (1985). Light-dependent antibody labelling of photoreceptors. Nature 316, 630–633.CrossRefGoogle ScholarPubMed
Barnstable, C.J. (1991). Molecular aspects of development of mammalian optic cup and formation of retinal cell types. Progress in Retinal Research 10, 45–67.CrossRefGoogle Scholar
Bonting, S.L., Caravaggio, L.L. & Gouras, P. (1961). The rhodopsin cycle in the developing vertebrate retina. I. Relation of rhodopsin content, electroretinogram, and rod structure in the rat. Experimental Eye Research 1, 14–24.CrossRefGoogle ScholarPubMed
Carter-Dawson, L.D., Alvarez, R.A., Fong, S.L., Liou, G.I., Sperling, H.G. & Bridge, C.D.B. (1986). Rhodopsin 11-cis-vitamin A, and interstitial retinol-binding protein (IRBP) during retinal development in normal and rd-mutant mice. Developmental Biology 116, 431–438.CrossRefGoogle Scholar
Carter-Dawson, L.D. & Vail, M.La (1979). Rods and cones in the mouse retina. II. Journal of Comparative Neurology 188, 263–272.CrossRefGoogle Scholar
Cicerone, C.M. (1976). Cones survive rods in the light damaged albino rat. Science 194, 1183–1185.CrossRefGoogle ScholarPubMed
Robertis, E.De (1960). Some observations on the ultrastructure and morphogenesis of photoreceptors. Journal of General Physiology (Suppl.) 43, 1–13.CrossRefGoogle Scholar
Deterre, P., Bigay, J., Forquet, F., Robert, M. & Chabre, M. (1988). cGMP phosphodiesterase of retinal rods is regulated by two inhibitory subunits. Proceedings of the National Academy of Sciences of the U.S.A. 85, 2424–2428.CrossRefGoogle ScholarPubMed
Eisenfeld, A.J., Bunt-Milam, A.H. & Saari, J.C. (1985). Immunocytochemical localization of interphotoreceptor retinoid-binding protein in developing normal and RCS rat retinas. Investigative Ophthalmology and Visual Science 26, 775–778.Google ScholarPubMed
Erdos, J.J., Tamtr, H., Barnstable, C.J. & Northup, J.K. (1989). Specificity and selectivity of polyclonal antisera against components of the neural and visual transduction pathways in rat and human retina histologic sections. Society for Neuroscience Abstracts 15, 205.Google Scholar
Farber, D.B., Park, S. & Yamashtta, C. (1988). Cyclic GMP phosphodiesterase of rd retina: Biosynthesis and content. Experimental Eye Research 46, 363–374.CrossRefGoogle ScholarPubMed
Fesenko, E.E., Kolesnikov, S.S. & Lyubarsky, S.S. (1985). Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310–313.CrossRefGoogle ScholarPubMed
Galbavy, E.S.J. & Olson, M.D. (1979). Morphogenesis of rod cells in the retina of the albino rat: A scanning electron microscopic study. Anatomical Record 195, 707–718.CrossRefGoogle Scholar
Hicks, D. & Barnstable, C. (1987 a). Different rhodopsin monoclonal antibodies reveal different binding patterns on developing and adult rat retina. Journal of Histochemistry and Cytochemistry 35, 1317–1328.CrossRefGoogle ScholarPubMed
Hicks, D. & Barnstable, C. (1987 b). A phosphorylation-sensitive antirhodopsin monoclonal antibody reveals light-induced phosphorylation of rhodopsin in the photoreceptor cell body. European Journal of Cell Biology 44, 341–347.Google ScholarPubMed
Hicks, D., Sparrow, J. & Barnstable, C.J. (1989). Immunoelectron microscopical examination of the surface distribution of opsin in rat rod photoreceptor cells. Experimental Eye Research 49, (1), 13–29.CrossRefGoogle ScholarPubMed
Ho, A.K., Somers, R.L. & Klein, D.C. (1986). Development and regulation of rhodopsin kinase in rat pineal and retina. Journal of Neurochemistry 46, 1176–1179.CrossRefGoogle ScholarPubMed
Horsburgh, G.M. & Sefton, A.J. (1987). Cellular degeneration and synaptogenesis in the developing retina of the rat. Journal of Comparative Neurology 263, 553–566.CrossRefGoogle ScholarPubMed
Hurwitz, R.L., Bunt-Milam, A.H. & Beavo, J.A. (1984). Immunological characterization of the photoreceptor outer segment cyclic GMP phosphodiesterase. Journal of Biological Chemistry 259, 8612–8618.CrossRefGoogle ScholarPubMed
Hurwitz, R.L., Bunt-Milam, A.H., Chang, M.L. & Beavo, J.A. (1985). cGMP phosphodiesterase in rod and cone outer segments of the retina. Journal of Biological Chemistry 260, 568–573.CrossRefGoogle ScholarPubMed
Vail, M.La (1973). Kinetics of rod outer segment renewal in the developing mouse retina. Journal of Cell Biology 58, 650–661.Google Scholar
Nir, I., Cohen, D. & Papermaster, D.S. (1984). Immunocytochemical localization of opsin in cell membrane of developing rat photoreceptors. Journal of Cell Biology 98, 1788–1795.CrossRefGoogle Scholar
Olney, J.W. (1968). An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Investigative Ophthalmology 7, 250–268.Google ScholarPubMed
Papermaster, D.S., Schneider, B.G. & Besharse, J.C. (1985). Vesicular transport of newly synthesized opsin from the Golgi apparatus toward the rod outer segment. Investigative Ophthalmology and Visual Science 26, 1386–1404.Google ScholarPubMed
Ratto, G.M., Robinson, D.W., Yan, B. & Mcnaughton, P.A. (1991). Development of the light response in neonatal mammalian rods. Nature 351, 654–657.CrossRefGoogle ScholarPubMed
Sharma, R.K. & Wang, J.H. (1985). Differential regulation of bovine brain calmodulindependent cyclic nucleotide phosphodiesterase isozymes by cyclic AMP-dependent protein kinase and calmodulindependent phosphatase. Proceedings of the National Academy of Sciences of the U.S.A. 82, 2603–2607.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756.CrossRefGoogle ScholarPubMed
Shaw, G. & Weber, K. (1983). The structure and development of the rat retina: An immunofluorescence microscopical study using antibodies specific for intermediate filament proteins. European Journal of Cell Biology 30, 219–232.Google ScholarPubMed
Shaw, G. & Weber, K. (1984). The intermediate filament complement of the retina: A comparison between different mammalian species. European Journal of Cell Biology 33, 95–104.Google ScholarPubMed
Shu, S., Ju, G. & Fan, L. (1988). The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neuroscience Letters 85, 169–171.CrossRefGoogle ScholarPubMed
Stryer, L. (1986). Cyclic GMP cascade of vision. Annual Review of Neuroscience 9, 87–119.CrossRefGoogle ScholarPubMed
Treisman, J.E., Morabito, M.A. & Barnstable, C.J. (1988). Opsin expression in the rat retina is developmentally regulated by transcriptional activation. Molecular and Cell Biology 8, 1570–1579.Google ScholarPubMed
Watanabe, T. & Raff, M.C. (1990). Rod photoreceptor development in vitro: Intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina. Neuron 2, 461–467.CrossRefGoogle Scholar
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. An electron microscopic study. Archives of Ophthalmology 79, 470–484.CrossRefGoogle ScholarPubMed
Weidman, T.A. & Kuwabara, T. (1969). Development of the rat retina. Investigative Ophthalmology 8, 60–69.Google ScholarPubMed