Abstract
Cyclic-GMP, which plays a pivotal role in visual transduction in the vertebrate retina, is synthesized by guanylate cyclase. The purpose of this study was to localize a rod outer segment-derived particulate guanylate cyclase (ROS-GC) to the retina of several species that have different populations of rods and cones. A rabbit antibody was raised against a synthetic peptide, corresponding to the sequence A107-L125 of bovine ROS-GC.
Western blot analysis showed a single immunoreactive band at about 115 kDa with bovine rod outer segments but not with human rod outer segments. Light microscopic immunocytochemistry of tissue sections revealed immunoreactivity in the outer segment layer and in the outer and inner plexiform layers. The rod-rich rat retina showed uniform immunolabeling of outer segments; the cone-containing cat retina showed heavily labeled cone outer segments and lighter labeling of rod outer segments; the cone-rich chicken retina showed a uniformly and intensely labeled outer segment layer. Preincubation of the primary antibody with the peptide completely blocked antibody binding.
Electron microscopic immunocytochemistry of the cat retina confirmed the presence of guanylate cyclase in photoreceptor outer segments and demonstrated its association with disk and plasma membranes. These data support a concept in which guanylate cyclase is much more concentrated in the outer segments of cones than rods. The immunolabeling of the plexiform layers suggests that the particulate guanylate cyclase is not unique to the photoreceptor outer segments, and may also play a role in transduction processes of retinal synapses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad I., Redmond L. J., and Barnstable C. J. (1990) Developmental and tissue-specific expression of the rod photoreceptor cGMP-gated ion channel gene.Biochem. Biophys. Res. Commun. 173, 463–470.
Ahmad I. and Barnstable C. J. (1993) Differential laminar expression of particulate and soluble guanylate cyclase genes in rat retina.Exp. Eye Res. 56, 51–62.
Barnstable C. J. (1980) Monoclonal antibodies which recognize different cell types in the retina.Nature 286, 231–235.
Braekevelt C. R. (1990) Fine structure of the retinal receptors of the domestic cat.Anat. Histol. Embryol. 19, 67–76.
de Azeredo F. A. M., Lust W. D., and Passonneau J. V. (1981) Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers.J. Biol. Chem. 256, 2731–2735.
Dizhoor A. M., Lowe D. G., Olshevskaya E. V., Laura R. P., and Hurley J. B. (1994) The human photoreceptor membrane guanylate cyclase, RetGC, is present in outer segments and is regulated by a calcium and a soluble activator.Neuron 12, 1–20.
Duda T., Goraczniak R. M., Sitaramayya A., and Sharma R. K. (1993) Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase.Biochemistry 32, 1391–1395.
Garbers D. L. (1990) The guanylyl cyclase receptor family.New Biol. 2, 499–504.
Goraczniak R. M., Duda T., Sitaramayya A., and Sharma R. K. (1994) Structural and functional characterization of rod outer segment membrane guanylate cyclase.Biochemistry 302, 455–461.
Krebs W. and Friedrich I. (1982) Quantitative morphology of bovine retina, inThe Structure of the Eye (Hollyfield J. G., ed.), Elsevier, New York, pp. 175–182.
La Vail M. M. (1976) Survival of some photoreceptor cells in albino rats following long-term exposure to continuous light.Invest. Ophthalmol. Vis. Sci. 15, 64–70.
Leon A. and Curtis R. (1990) Autosomal dominant rod-cone dyslasia in theRdy cat. 1. Light and electron microscope findings.Exp. Eye Res. 51, 361–381.
Liu X. R., Seno K., Nishizawa Y., Hayashi F., Yamazaki A., Matsumoto H., Wakabayashi T., and Usukura J. (1994) Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas.Exp. Eye Res. 59, 761–768.
Margulis A., Goraczniak R. M., Duda T., Sharma R. K., and Sitaramayya A. (1993) Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase.Biochem. Biophys. Res. Commun. 194, 855–861.
Mariani A. P. and Leure-DuPree A. E. (1978) Photoreceptors and oil droplet colors in the red area of the pigeon retina.J. Comp. Neurol. 182, 821–838.
Meyer D. B. and May H. C., Jr. (1973) The topographical distribution of rods and cones in the adult chicken retina.Exp. Eye Res. 17, 347–355.
Miller J. L., Picones A., and Korenbrot J. I. (1994) Differences in transduction between rods and cone photoreceptors: an exploration of the role of calcium homeostasis.Curr. Opin. Neurobiol. 4, 488–495.
Morris V. B. and Shorey C. D. (1967) An electron microscope study of types of receptor in the chick retina.J. Comp. Neurol. 129, 313–340.
Nawy S. and Jahr C. E. (1991) cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter.Neuron 7, 677–683.
Orr H. T., Lowry O. H., Cohen A. I., and Ferrendelli J. A. (1976) Distribution of 3′:5′-cyclic AMP and 3′:5′-cyclic GMP in rabbit retina in vivo: selective effects of dark and light adaptation and ischemia.Proc. Natl. Acad. Sci. 73, 4442–4445.
Pozdnyakov N., Yoshida A., Cooper N. G. F., Margulis A., Duda T., Sharma R. K., and Sitaramayya A. (1995) A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase.Biochemistry 34, 14,279–14,283.
Pugh E. N. Jr. and Lamb T. D. (1993) Amplification and kinetics of the activation steps in phototransduction.Biochem. Biophys. Acta 1141, 111–149.
Rieke F. and Schwartz E. A. (1994) A cGMP-gated current can control exocytosis at cone synapses.Neuron 13, 863–873.
Shyjan A. W., de-Saauvage F. J., Gillett N. A., Goeddel D. V., and Lowe D. G. (1992) Molecular cloning of a retina-specific membrane guanylate cyclase.Neuron 9, 727–737.
Smith R. G., Freed M. A., and Sterling P. (1986) Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network.J. Neurosci. 6, 3505–3517.
Stryer L. (1991) Visual excitation and recovery.J. Biol. Chem. 266, 10,711–10,714.
Yang R.-B., Foster D. C., Garbers D. L., and Fulle H.-J. (1995) Two membrane forms of guanylyl cyclase found in the eye.Proc. Natl. Acad. Sci. USA 92, 602–606.
Yoshida A., Cooper N. G. F., Liu L., Pozdnyakov N., and Sitaramayya A. (1995) Localization of photoreceptor membrane guanylate cyclase.Invest. Ophthalmol. Vis. Sci. 36, S270.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cooper, N., Liu, L., Yoshida, A. et al. The bovine rod outer segment guanylate cyclase, ROS-GC, is present in both outer segment and synaptic layers of the retina. J Mol Neurosci 6, 211–222 (1995). https://doi.org/10.1007/BF02736766
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02736766