Abstract
The possible involvement of phosphodiesterase (PDE) activation in phototransduction was investigated in gecko photoreceptors by comparing the in situ PDE activity with the photoreceptor potential. In the dark, intracellular injection of cGMP into a gecko photoreceptor caused a long-lasting depolarization. An intense light flash given during the depolarization phase repolarized the cell with a short latency comparable to that of the light-evoked hyperpolarizing response, which indicates that the activation of PDE in situ is rapid enough to generate the photoreceptor potential. PDE activity in situ was estimated quantitatively from the duration of the cGMP-induced depolarization, since it was expected that the higher the PDE activity, the shorter the duration. Under steady illumination, the enzyme exhibited a constant activity. On exposure to a light flash, PDE became activated, but recovered in the dark with a time course that was dependent on the intensity of the preceding stimulus. When PDE activity and photoreceptor sensitivity to light were measured in the same cell after a light flash, both recovery processes showed similar kinetics. Theoretical analysis showed that the parallelism in the recovery time courses could be explained if cGMP is the transduction messenger. These results suggest that PDE activation is involved not only in the generation but also in the adaptation mechanisms of the photoreceptor potential.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baylor D. A., Hodgkin A. L. Changes in time scale and sensitivity in turtle photoreceptors. J Physiol. 1974 Nov;242(3):729–758. doi: 10.1113/jphysiol.1974.sp010732. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baylor D. A., Matthews G., Nunn B. J. Location and function of voltage-sensitive conductances in retinal rods of the salamander, Ambystoma tigrinum. J Physiol. 1984 Sep;354:203–223. doi: 10.1113/jphysiol.1984.sp015372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biernbaum M. S., Bownds M. D. Frog rod outer segments with attached inner segment ellipsoids as an in vitro model for photoreceptors on the retina. J Gen Physiol. 1985 Jan;85(1):83–105. doi: 10.1085/jgp.85.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brin K. P., Ripps H. Rhodopsin photoproducts and rod sensitivity in the skate retina. J Gen Physiol. 1977 Jan;69(1):97–120. doi: 10.1085/jgp.69.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cote R. H., Biernbaum M. S., Nicol G. D., Bownds M. D. Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors. J Biol Chem. 1984 Aug 10;259(15):9635–9641. [PubMed] [Google Scholar]
- Fain G. L., Gerschenfeld H. M., Quandt F. N. Calcium spikes in toad rods. J Physiol. 1980 Jun;303:495–513. doi: 10.1113/jphysiol.1980.sp013300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fain G. L., Lisman J. E. Membrane conductances of photoreceptors. Prog Biophys Mol Biol. 1981;37(2):91–147. doi: 10.1016/0079-6107(82)90021-9. [DOI] [PubMed] [Google Scholar]
- Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
- Fleischman D., Denisevich M., Raveed D., Pannbacker R. G. Association of guanylate cyclase with the axoneme of retinal rods. Biochim Biophys Acta. 1980 Jun 19;630(2):176–186. doi: 10.1016/0304-4165(80)90419-5. [DOI] [PubMed] [Google Scholar]
- Fukada Y., Yoshizawa T. Activation of phosphodiesterase in frog rod outer segment by an intermediate of rhodopsin photolysis. II. Biochim Biophys Acta. 1981 Jul;675(2):195–200. doi: 10.1016/0304-4165(81)90226-9. [DOI] [PubMed] [Google Scholar]
- Goldberg N. D., Ames A. A., 3rd, Gander J. E., Walseth T. F. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J Biol Chem. 1983 Aug 10;258(15):9213–9219. [PubMed] [Google Scholar]
- Kawamura S., Bownds M. D. Light adaption of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions. J Gen Physiol. 1981 May;77(5):571–591. doi: 10.1085/jgp.77.5.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawamura S. Involvement of ATP in activation and inactivation sequence of phosphodiesterase in frog rod outer segments. Biochim Biophys Acta. 1983 Jul 13;732(1):276–281. doi: 10.1016/0005-2736(83)90212-2. [DOI] [PubMed] [Google Scholar]
- Kawamura S., Murakami M. Functional role of phosphodiesterase in gecko photoreceptors. Neurosci Res Suppl. 1985;2:S119–S125. doi: 10.1016/0921-8696(85)90011-8. [DOI] [PubMed] [Google Scholar]
- Kawamura S., Murakami M. Intracellular injection of cyclic-GMP increases sodium conductance in gecko photoreceptors. Jpn J Physiol. 1983;33(5):789–800. doi: 10.2170/jjphysiol.33.789. [DOI] [PubMed] [Google Scholar]
- Kilbride P., Ebrey T. G. Light-initiated changes of cyclic guanosine monophosphate levels in the frog retina measured with quick-freezing techniques. J Gen Physiol. 1979 Sep;74(3):415–426. doi: 10.1085/jgp.74.3.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Korenbrot J. I. Signal mechanisms of phototransduction in retinal rod. CRC Crit Rev Biochem. 1985;17(3):223–256. doi: 10.3109/10409238509113605. [DOI] [PubMed] [Google Scholar]
- Liebman P. A., Sitaramayya A. Role of G-protein-receptor interaction in amplified phosphodiesterase activation of retinal rods. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;17:215–225. [PubMed] [Google Scholar]
- MacLeish P. R., Schwartz E. A., Tachibana M. Control of the generator current in solitary rods of the Ambystoma tigrinum retina. J Physiol. 1984 Mar;348:645–664. doi: 10.1113/jphysiol.1984.sp015131. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matthews H. R., Torre V., Lamb T. D. Effects on the photoresponse of calcium buffers and cyclic GMP incorporated into the cytoplasm of retinal rods. Nature. 1985 Feb 14;313(6003):582–585. doi: 10.1038/313582a0. [DOI] [PubMed] [Google Scholar]
- Miki N., Keirns J. J., Marcus F. R., Freeman J., Bitensky M. W. Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3820–3824. doi: 10.1073/pnas.70.12.3820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller W. H. Physiological evidence that light-mediated decrease in cyclic GMP is an intermediary process in retinal rod transduction. J Gen Physiol. 1982 Jul;80(1):103–123. doi: 10.1085/jgp.80.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinto L. H., Brown J. E. Pressure injection of 3',5'-cyclic GMP into solitary rod photoreceptors of the tiger salamander. Brain Res. 1984 Jun 18;304(1):197–200. doi: 10.1016/0006-8993(84)90882-5. [DOI] [PubMed] [Google Scholar]
- Polans A. S., Kawamura S., Bownds M. D. Influence of calcium on guanosine 3',5'-cyclic monophosphate levels in frog rod outer segments. J Gen Physiol. 1981 Jan;77(1):41–48. doi: 10.1085/jgp.77.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson P. R., Kawamura S., Abramson B., Bownds M. D. Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. J Gen Physiol. 1980 Nov;76(5):631–645. doi: 10.1085/jgp.76.5.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwartz E. A. Phototransduction in vertebrate rods. Annu Rev Neurosci. 1985;8:339–367. doi: 10.1146/annurev.ne.08.030185.002011. [DOI] [PubMed] [Google Scholar]
- Stryer L. Transducin and the cyclic GMP phosphodiesterase: amplifier proteins in vision. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):841–852. doi: 10.1101/sqb.1983.048.01.087. [DOI] [PubMed] [Google Scholar]
- Woodruff M. L., Bownds M. D. Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3',5'-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol. 1979 May;73(5):629–653. doi: 10.1085/jgp.73.5.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamazaki A., Sen I., Bitensky M. W., Casnellie J. E., Greengard P. Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J Biol Chem. 1980 Dec 10;255(23):11619–11624. [PubMed] [Google Scholar]
- Yamazaki A., Uchida S., Stein P. J., Wheeler G. L., Bitensky M. W. Enzyme regulation and GTP binding protein: an algorithm of control that includes physical displacement of an inhibitory protein. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;16:381–392. [PubMed] [Google Scholar]
- Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
- Yau K. W., Nakatani K. Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature. 1985 Sep 19;317(6034):252–255. doi: 10.1038/317252a0. [DOI] [PubMed] [Google Scholar]
- Yee R., Liebman P. A. Light-activated phosphodiesterase of the rod outer segment. Kinetics and parameters of activation and deactivation. J Biol Chem. 1978 Dec 25;253(24):8902–8909. [PubMed] [Google Scholar]
- de Azeredo F. A., Lust W. D., Passonneau J. V. Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers. J Biol Chem. 1981 Mar 25;256(6):2731–2735. [PubMed] [Google Scholar]