Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors.

Payne, Richard; Corson, D. Wesley; Fein, Alan M.

doi:10.1085/jgp.88.1.107

Cited by 120 publications

(64 citation statements)

References 31 publications

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“…While under steady state conditions free cytosolic calcium im pairs the generation of single-photon responses, some rapid (probably local) increase in Caj ap pears obligatory to evoke them. Indeed, calcium led to depolarization of the photoreceptor only when pressure-injected (Payne et al, 1986b), not when applied ionophoretically (Lisman and Brown, 1972).…”

Section: Effect O F Calcium On Response Generation and Adaptationmentioning

confidence: 98%

“…More controversially discussed is the role of calcium ions in the excitation process. Injection of M. D orlöchter et al ■ Calcium -Independent Photoresponse in Lim ulus Ventral Photoreceptor 447 calcium into ventral photoreceptors increased the light response in calcium-deprived cells, or elicited inward currents similar to those caused by light so that an obligatory role for calcium in excitation was proposed (Bolsover and Brown, 1985;Payne, Corson and Fein, 1986b;Shin, Richard and Lisman, 1993). On the other hand, application of calcium buffer or agents blocking calcium release did not completely inhibit the photocurrent indi cating calcium-independent initiation of a light re sponse (Frank and Fein, 1991;Contzen, Richter and Nagy, 1995).…”

Section: Introductionmentioning

confidence: 99%

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Effects of Calcium and Cyclopiazonic Acid on the Photoresponse in the Limulus Ventral Photoreceptor

Dorlöchter

Yuan

Stieve

1999

Zeitschrift Für Naturforschung C

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Phototransduction, Current Components, Light Adaptation, Bumps, CPA 1. Single-photon responses (bumps) and small macroscopic photocurrents were studied in ventral photoreceptors of the horseshoe crab Limulus. Lowering the calcium concentration in the bath from 10 mM to 250 fiM led to increased bump size. Adaptation of the cells by a moderately bright conditioning flash was not impaired.2. Pressure-injection of 1.2 mM EG TA into the dark-adapted cells resulted in reduced bump size. EG TA weakened the effect of the conditioning light flash although it did not completely abolish light adaptation.3. The microsomal calcium-ATPase inhibitor cyclopiazonic acid strongly desensitized the cells, and bumps were suppressed below detection. When the bathing saline contained 10 m M calcium, macroscopic photoresponses after extracellular application of the agent had ampli tudes smaller than under control conditions but normal response kinetics: The response to a light step still consisted of a fast transient photocurrent and a much smaller plateau. How ever, when applied in calcium-free bathing saline, cyclopiazonic acid additionally influenced the waveform of the photoresponse. The clear distinction between transient and plateau was no longer possible, and the photocurrent appeared "square".4. Our results support the idea that a transient elevation of the cytosolic calcium concentra tion is obligatory for light adaptation in the ventral photoreceptor. It is also obligatory for the generation of the so-called C2 component of the photocurrent which is represented by "standard" bumps and the fast transient phase of a prolonged response. However, a rise in cytosolic calcium appears not necessary for the initiation of a slow electrical photoresponse.

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Section: Effect O F Calcium On Response Generation and Adaptationmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Effects of Calcium and Cyclopiazonic Acid on the Photoresponse in the Limulus Ventral Photoreceptor

Dorlöchter

Yuan

Stieve

1999

Zeitschrift Für Naturforschung C

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“…Third, although PKC inhibitors slightly sensitize the photoresponse and antagonize the effect of PKC activators, they do not reverse the decrease in sensitivity associated with light adaptation for the adaptation protocols that we describe. Finally, injection of calcium ions alone into the photoreceptor can f ully mimic light adaptation (Brown and Lisman, 1975;Fein and Charlton, 1977) and suppress the response to InsP 3 (Payne et al, 1986a) without any requirement for the addition of DAG or a surrogate. However, each of these results is subject to caveats, and it is not possible to conclude from these results that PKC plays no role in adaptation.…”

Section: Pkc Activators Do Not Mimic Light Adaptation Nor Do Pkc Inhmentioning

confidence: 99%

Protein Kinase C Activators Inhibit the Visual Cascade inLimulusVentral Photoreceptors at an Early Stage

Dabdoub

Payne

1999

J. Neurosci.

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The phosphoinositide cascade mediates visual transduction in invertebrate photoreceptors. Phospholipase C (PLC) catalyzes the hydrolysis of phosphatidylinositol bisphosphate, producing inositol trisphosphate (InsP 3 ) and diacylglycerol (DAG). Protein kinase C (PKC) is a major target of DAG in many cell types. We have used PKC activators to investigate the function of the kinase in the phototransduction cascade in Limulus polyphemus ventral photoreceptors. Extracellular application of (Ϫ)-indolactam V (0.03-30 M) or phorbol-12,13-dibutyrate (10 M) reversibly reduced the sensitivity of the electrical response of the photoreceptors to light by up to 1000-fold. The inert stereoisomer (ϩ)-indolactam V and 4␣-phorbol had no effect. The effect of (Ϫ)-indolactam V was antagonized by the PKC inhibitors bisindolylmaleimide I and Gö 6976. Coapplication of bisindolylmaleimide V, used as a negative control compound for PKC inhibition, did not reduce the effectiveness of (Ϫ)-indolactam V. These findings are consistent with (Ϫ)-indolactam V activating PKC and desensitizing the light response. Furthermore, our pharmacological results indicate that PKC activation does not appear to play a role in light adaptation. We localized the position of the target of PKC in the visual cascade. We chemically excited the cascade at various stages to determine the kinase's target. PKC activation by (Ϫ)-indolactam V decreased the light-induced elevation of intracellular calcium but had no effect on the photoreceptor's excitatory response to intracellular injection of InsP 3 . However, the PKC activator greatly reduced the excitation caused by GTP-␥-S injection. We propose that PKC inhibits the visual transduction cascade at the G-protein and/or PLC stage.

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“…Robinson, Wood, Szuts, Fein, Hamm & Lisman (1990) recently reported that three different light-activated G-proteins exist in squid photoreceptors. Payne et al (1986a) have shown that calcium injection induces a membrane current in Limulus ventral nerve photoreceptor similar to that induced by light. Buffering the intracellular calcium does not completely block the light-induced response, although it blocks the calcium-induced response.…”

Section: Introductionmentioning

confidence: 95%

Three components in the light‐induced current of the Limulus ventral photoreceptor.

Deckert

Nagy

Helrich

et al. 1992

The Journal of Physiology

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SUMMARY1. Light-induced currents were measured in Limulus ventral nerve photoreceptors using a two-electrode voltage clamp. Three kinetically distinct components in the light-induced current could be distinguished by varying the light adaptation state of the photoreceptor and the intensity of the stimulus light.2. The components could be partly separated by choosing appropriate stimulus intensities and dark adaptation time. Thus the properties of the components could be separately studied. The first component is the first to recover after a light adaptation, appears temporally first in the light-induced response, has the lowest activation threshold and is the smallest. The second component needs a longer time to recover after an adapting illumination and its kinetics differ from that of the other components. Applying a bright stimulus to a dark-adapted cell a third component can be observed late in the response.3. The time to peak of the first and the third components depended on the stimulus intensity, but not on the dark adaptation time. The time to peak of the second component became shorter the longer the dark adaptation time. For a constant adaptation state the time to the maximum of component 2 was independent, but those of components 1 and 3 were dependent on the membrane voltage.4. To exclude the possibility of the contribution of voltage-gated currents, lightactivated currents were measured at clamp potentials more negative than -50 mV after adding 4-aminopyridine into the bath solution or injecting tetraethylammonium chloride into the cell. The properties of the three components remained unchanged under these conditions. 5. The I-V curve of the first component was flat at negative membrane potentials and had a strong outward rectification at positive membrane potentials. The I-V curve of component 3 showed a negative resistance at potentials more negative than about -30 mV. In contrast, the I-V curve for the second component was always nearly linear.6. No membrane potential was found where the light-induced current was zero.Instead, current traces close to the reversal potential showed a complex waveform indicating different reversal potentials for the three components.

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Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors.

Cited by 120 publications

References 31 publications

Effects of Calcium and Cyclopiazonic Acid on the Photoresponse in the Limulus Ventral Photoreceptor

Effects of Calcium and Cyclopiazonic Acid on the Photoresponse in the Limulus Ventral Photoreceptor

Protein Kinase C Activators Inhibit the Visual Cascade inLimulusVentral Photoreceptors at an Early Stage

Three components in the light‐induced current of the Limulus ventral photoreceptor.

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