Single-channel recordings demonstrate that cGMP opens the light-sensitive ion channel of the rod photoreceptor.

Matthews, Gary

doi:10.1073/pnas.84.1.299

Cited by 65 publications

(54 citation statements)

References 19 publications

(23 reference statements)

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“…The difference spectrum of the cyclic GMPactivated channel was obtained by subtracting the power spectrum during perfusion of the inner face of the membrane with 0 Ca2 +, 0 Mg2 + Ringer solution from the spectrum during perfusion with 0 Ca2+, 0 Mg2' Ringer solution + 10 /LM-cyclic GMP. As shown by Matthews (1987) the two difference spectra were superimposable, suggesting that the two channels had the same over-all kinetics. Both spectra could be described by a sum of two Lorentzian components, with corner frequencies of 75 + 8 and 1080 + 120 Hz for the light-sensitive channel and 85 + 5 and 1000 + 130 Hz for the cyclic GMP-activated channel.…”

Section: Effect Of Non-saturating Illumination On Temporal Propertiesmentioning

confidence: 83%

“…In a number of experiments, it proved possible to excise a patch in inside-out configuration after recording light-sensitive channel activity in the same patch while it was still attached to the rod. Those experiments allowed a direct comparison of light-sensitive and cyclic GMP-activated channels in the same membrane (Matthews, 1987). Samples of channel activity from one such experiment are shown in Fig.…”

Section: Effect Of Non-saturating Illumination On Temporal Propertiesmentioning

confidence: 99%

“…An abstract (Matthews, 1986d) and a brief preliminary report (Matthews, 1987) of some of the results presented here have appeared.…”

Section: Introductionmentioning

confidence: 99%

“…However, there is evidence that external Ca2+ blocks the light-sensitive channel (Bodoia & Detwiler, 1984b;Matthews, 1985b), which suggests that removal of divalent cations from the extracellular fluid might increase the single-channel current sufficiently to allow resolution of single channels. In addition, recent data show that Ca2' and Mg2+ reduce the amplitude of the cyclic GMP-activated conductance of excised patches of rod membrane Matthews, 1986a;Haynes, Kay & Yau, 1986;Zimmerman & Baylor, 1986) and that removal of divalent cations permits single-channel recordings from the cyclic GMP-sensitive conductance (Haynes, Kay & Yau, 1986;Zimmerman & Baylor, 1986; Matthews, 1986dMatthews, , 1987. In the experiments reported here, cell-attached patch-clamp recordings were made from intact, dark-adapted rod photoreceptors using patch pipettes filled with Ringer solution lacking divalent cations.…”

Section: Introductionmentioning

confidence: 99%

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Properties of ion channels closed by light and opened by guanosine 3',5'‐cyclic monophosphate in toad retinal rods.

Matthews

Watanabe

1987

The Journal of Physiology

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SUMMARY1. In patch-clamp recordings from outer segments of dark-adapted rod photoreceptors, single-channel recordings were obtained from the light-sensitive conductance when divalent cations were omitted from the pipette solution bathing the extracellular face of the recorded patch of membrane.2. Activity of the light-sensitive channel was suppressed by light within the normal response range of the dark-adapted rod. During dim, steady illumination, the rate of opening of the channel fluctuated dramatically, as expected qualitatively from statistical fluctuations in the number of photoisomerizations occurring within the effective collecting area of the recorded patch.3. The light-sensitive channel flickered rapidly in the open state, so that individual events appeared as a burst of openings and closings. The average duration of a burst was 0-78+0-03 ms (mean+ s.E.). The average duration of an individual opening was 0 18 + 0008 ms. The average closed duration within a burst was 0-37 + 0-02 ms.4. Hyperpolarization of the recorded patch had no effect on average burst or open duration, although opening frequency increased slightly (+ 18-6 + 4-9%; n = 13; mean+ S.E.). Average single-channel current increased linearly with hyperpolarization, giving an estimated single-channel conductance of 20-5 + 1F1 pS. By extrapolation of the relation between channel current and hyperpolarization, the dark driving force was estimated to be about 48 mV.5. In addition to reducing the rate of channel events, dim non-saturating light also reduced the average duration of a burst of openings and the average duration of openings within a burst.6. About 50 % of cell-attached patches showed no channel activity in darkness.

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Section: Effect Of Non-saturating Illumination On Temporal Propertiesmentioning

confidence: 83%

Section: Effect Of Non-saturating Illumination On Temporal Propertiesmentioning

confidence: 99%

“…An abstract (Matthews, 1986d) and a brief preliminary report (Matthews, 1987) of some of the results presented here have appeared.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Properties of ion channels closed by light and opened by guanosine 3',5'‐cyclic monophosphate in toad retinal rods.

Matthews

Watanabe

1987

The Journal of Physiology

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“…Furthermore, in all of these preparations, the presence of divalent cations in the extracellular milieu is inhibitory. Insofar as estimates of elementary conductance underlying the CAMP-induced inward currents in these various preparations have been made, they appear to be remarkably similar: 20-25 pS for the current seen in photoreceptors [bathed in divalent-free intracellular and extracellular solutions (e.g., Matthews, 1987;Haynes et al, 1986)], compared to 20 pS for the only published estimate of the elementary conductance underlying the molluscan CAMP-induced slow inward current [Green and Gillette, 1983 (made in normal seawater)]. Furthermore, the concentration of the cyclic nucleotide required for activating the current in the different preparations is in the micromolar range for all 3 of the preparations for which an estimate has been made (photoreceptors: Fesenko et al, 1985;Haynes et al, 1986; olfactory receptor cilia: Nakamura and Gold, 1987;molluscan neurons: Connor and Hockberger, 1984a;Hockberger and Yamane, 1987).…”

Section: +25mentioning

confidence: 99%

Cyclic AMP-induced slow inward current in depolarized neurons of Aplysia californica

Kehoe

1990

J. Neurosci.

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Cyclic nucleotides have been implicated in many long-lasting transmitter-induced effects on membrane conductance. One previously observed effect of cAMP on molluscan neurons is to induce a slow inward current, which has been further evaluated here in depolarized anterior and medial cells of the pleural ganglion of Aplysia californica in order to understand better its underlying ionic mechanisms and its sensitivity to a variety of pharmacological agents. This current, which appears to be the only cAMP-induced current seen in the anterior cells, was shown to invert at about +25 mV, that is, approximately 25-30 mV inferior to ENa. This reversal potential was lowered by about 15-16 mV when half of the extracellular Na was replaced by either mannitol or N- methyl-D-glucamine, whereas it was unaffected by changes in extracellular Cl, Ca, or Mg. The response persisted in seawater in which the Na had been totally replaced by K, and its reversal potential shifted towards more negative values. These data are consistent with the hypothesis that both Na and K ions permeate the channel, with a Na/K permeability ratio of approximately 2. Ca ions do not appear to permeate the channel, but they do have a marked inhibitory effect on the response amplitude, as do Mg ions when Ca is not present. Caffeine, intracellular acidification, and phosphodiesterase inhibitors enhance and prolong the response without changing its reversal potential. Previous studies have shown that both caffeine and intracellular acidification inhibit phosphodiesterase, and it is assumed that the common effect of these manipulations on the cAMP-induced inward current is mediated, at least partially, by the inhibition of that enzyme. In the medial cells of the pleural ganglion, this slow inward current is present, but is dominated in the depolarized cell by a cAMP-induced diminution in a Ca-activated K conductance (Kehoe, 1985b). This K conductance and, consequently, the noninverting, cAMP-induced inward current that reflects its diminution, were shown to disappear in Ca- free solutions, in the presence of isobutyl-1-methylxanthine (IBMX) or caffeine, and upon acidification of the cytoplasm. When this cAMP- sensitive K conductance is blocked, the presence of the inverting cAMP- induced cationic current is unmasked. The cAMP-induced cationic current is shown to have many properties in common with cyclic nucleotide- induced currents described in photoreceptors, olfactory receptor cilia, and cardiac myocytes, all of which have been shown to be outwardly rectifying cationic currents that are inhibited by divalent cations and do not involve the activation of a cAMP-dependent kinase.

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The cGMP-Gated Channels of Rod and Cone Photoreceptors

Haynes

Yau

1990

Transduction in Biological Systems

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Single-channel recordings demonstrate that cGMP opens the light-sensitive ion channel of the rod photoreceptor.

Cited by 65 publications

References 19 publications

Properties of ion channels closed by light and opened by guanosine 3',5'‐cyclic monophosphate in toad retinal rods.

Properties of ion channels closed by light and opened by guanosine 3',5'‐cyclic monophosphate in toad retinal rods.

Cyclic AMP-induced slow inward current in depolarized neurons of Aplysia californica

The cGMP-Gated Channels of Rod and Cone Photoreceptors

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