Calcium effects on frog retinal cyclic guanosine 3', 5'-monophosphate levels and their light-initiated rate of decay.

Kilbride, Paul E.

doi:10.1085/jgp.75.4.457

Cited by 52 publications

(20 citation statements)

References 14 publications

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“…First, the procedures used to change the internal concentration of Ca2+ and cGMP may affect other cell functions (Bianchi, 1961;Sheppard, 1970;Plagemann, 1974;Gaska, Canter & Shelanski, 1975;Klausner, Bhalla, Dragsten, Hoover & Karnovsky, 1980). A second problem is that cGMP and Ca2+ may play interacting roles in rod physiology since changes in the concentration ofone change the concentration ofthe other (Cohen et al 1978;Kilbride & Ebrey, 1979;Kilbride, 1980;Polans et al 1981). Despite these complications, the present results can be used to help either validate or invalidate some of the currently popular models of photoreceptor excitation.…”

Section: Discussionmentioning

confidence: 93%

Effects of calcium and guanosine‐3',5'‐cyclic‐monophosphoric acid on receptor potentials of toad rods.

Waloga¹

1983

The Journal of Physiology

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SUMMARY1. Membrane potential was recorded intracellularly from rod outer segments in the isolated retina of Bufo marinUs. The composition of the solution flowing over the exposed receptor side of the retina was changed rapidly and ionophoretic injections were made into single rod outer segments.2. Lowering the external Ca2+ concentration, adding 3-isobutyl-1-methylxanthine (IBMX) to the bath, or ionophoretic injections of guanosine-3':5'-cyclic monophosphoric acid (cGMP) lead to depolarization of the rod membrane and an increase in the maximum peak amplitude of the receptor potential.3. Lowering the Ca2+ concentration or adding IBMX to the bath shifted the curve of response amplitude vs. log intensity of stimulus and a-(intensity at half saturation) towards dimmer intensities. The ionophoresis of cGMP did not shift the position of the curve along the log stimulus intensity axis.4. Changing the external concentration of Ca or IBMX changes the form of the response amplitude vs. log intensity curve. This is most obvious at dim intensities. The amplitude of receptor potentials elicited by dim light was decreased by lowering Ca but increased by IBMX. The kinetics of receptor potentials were affected differently by solutions with a low Ca2+ concentration and those containing IBMX. The recovery phase of the receptor potential was slightly accelerated in the low Ca solution, whereas it was greatly slowed in the IBMX-containing solution. The ionophoretic injection of cGMP also slowed the recovery of the receptor potential.5. The data presented do not support the proposal that cGMP alone maintains membrane voltage in the dark and that the light-induced hydrolysis of cGMP results in the light-induced decrease in membrane conductance underlying the receptor potential. It is more likely that both Ca2+ and cGMP interact in the modulation of membrane voltage, perhaps as interrelated messengers.

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Section: Discussionmentioning

confidence: 93%

Effects of calcium and guanosine‐3',5'‐cyclic‐monophosphoric acid on receptor potentials of toad rods.

Waloga¹

1983

The Journal of Physiology

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“…It was not the purpose of this investigation to explore possible functions of cyclic AMP in photoreceptor transduction or adaptation, but Lipton et al (1977) did find some physiological evidence for a possible antagonism of the cyclic AMP and cyclic GMP systems in photoreceptors, and the possible role of cyclic GMP in transduction and/or adaptation is under active investigation (Yee and Liebman, 1978;Liebman and Pugh, 1979;Woodruff and Bownds, 1979;Biernbaum and Bownds, 1979;Kilbride, 1980;Kawamura and Bownds, 1981).…”

Section: Discussionmentioning

confidence: 99%

Increased Levels of 3′,5′‐Cyclic Adenosine Monophosphate Induced by Cobaltous Ion or 3‐Isobutylmethylxanthine in the Incubated Mouse Retina: Evidence Concerning Location and Response to Ions and Light

Cohen

1982

Journal of Neurochemistry

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Dark levels of 3',5'-cyclic adenosine monophosphate (cyclic AMP) of mouse retinas incubated in Earle's medium were elevated by 3-isobutyl-methylxanthine (IBMX) and/or Co2+ or Mn2+, but not by Cd2+, methylverapamil, or excess Mg2+ of Ca2+. Light reduced elevated dark levels of cyclic AMP in the presence of agents known to block the light modulation of post-receptoral neurons (aspartate, Co2+, high Mg2+), a finding consistent with a cyclic AMP metabolism in photoreceptors. Co2+-elevated cyclic AMP levels were not less light-sensitive than cyclic GMP levels. Ouabain substantially increased IBMX-elevated cyclic AMP with a persistent light response, but reduced the dark action of Co2+. IBMX, but not Co2+, also increased cyclic AMP in receptorless (rd/rd) retinas; haloperidol partly reduced this IBMX effect. In normal retinas in Co2+ medium, progressively replacing Na+ by K+ (but not choline+) from 1--50 mM caused a progressive fall in dark, light-sensitive cyclic AMP levels, but from 50 to 100 mM-K+ there appeared haloperidol-preventable increases in both the dark- and light-insensitive levels of cyclic AMP. In IBMX-aspartate medium a haloperidol-preventable, light-insensitive increase in cyclic AMP appeared from 20 mM-K+ upwards. Haloperidol-preventable increases in cyclic AMP as induced by high K+ required Co2+ in normal retinas, but not in receptorless retinas, and 5 nM-Co2+ greatly increased the response to dopamine in receptorless retinas. The post-dopaminergic neurons, which are 4th-order neurons, may have become hypersensitive to dopamine in receptorless retinas consequent to the absent signal from the 1st-order photoreceptors, or directly, as an effect of the same gene underlying the dystrophy.

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“…The plausibility of these suggestions rests on demonstrating appropriate correlations between the kinetics of the phosphodiesterase, cyclic GMP, and conductance changes measured in living receptor cells, and thus far definitive experiments have not been done. Kilbride and Ebrey (1979) and Kilbride (1980) have shown that illumination causes cyclic GMP levels of whole retinas to fall over a period of seconds, rather than milliseconds. Lowering calcium concentration in the Ringer's solution from 1.6 mM to a nanomolar level increases the cyclic GMP change.…”

Section: Introductionmentioning

confidence: 99%

Light adaption of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions.

Kawamura¹,

Bownds²

1981

The Journal of General Physiology

120

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The light-activated guanosine 3',5'-cyclic monophosphate (cyclic GMP) phosphodiesterase (PDE) of frog photoreceptor membranes has been assayed by measuring the evolution of protons that accompanies cyclic GMP hydrolysis. The validity of this assay has been confirmed by comparison with an isotope assay used in previous studies (Robinson et al. 1980. J. Gen. Physiol. 76: 631-645). The PDE activity elicited by either flash or continuous dim illumination is reduced if ATP is added to outer segment suspensions. This desensitization is most pronounced at low calcium levels. In 10 -9 M Ca ++, with 0.5 mM ATP and 0.5 mM GTP present, PDE activity remains almost constant as dim illumination and rhodopsin bleaching continue. At intermediate Ca ++ levels (10 -7-10 -5 M) the activity slowly increases during illumination. Finally, in 10 -4-10 -3 M Ca ++ the sensitivity control exerted by ATP has almost disappeared, and PDE activity is more a reflection of the total number of rhodopsin molecules bleached than of the rate of the rhodopsin bleaching. At intermediate or low calcium levels a short-lived inhibitory process is revealed by observing a nonlinear summation of responses of the enzyme to closely spaced flashes of light. Each flash makes PDE activity less responsive to successive flashes, and a steady state is obtained in which activation and inactivation are balanced. It is suggested that calcium and ATP regulation of PDE play a role in the normal light adaptation processes of frog photoreceptor membranes.

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Calcium effects on frog retinal cyclic guanosine 3', 5'-monophosphate levels and their light-initiated rate of decay.

Cited by 52 publications

References 14 publications

Effects of calcium and guanosine‐3',5'‐cyclic‐monophosphoric acid on receptor potentials of toad rods.

Effects of calcium and guanosine‐3',5'‐cyclic‐monophosphoric acid on receptor potentials of toad rods.

Increased Levels of 3′,5′‐Cyclic Adenosine Monophosphate Induced by Cobaltous Ion or 3‐Isobutylmethylxanthine in the Incubated Mouse Retina: Evidence Concerning Location and Response to Ions and Light

Light adaption of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions.

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