Abstract
Ion channels in excised patches of plasma membrane are generally considered to be isolated from any intracellular regulation mechanisms. For example, in excised patches of vertebrate rod outer segment plasma membrane, the cGMP-activated cation channels have traditionally been studied in room light because the enzyme cascade linking photon absorption to channel closure was assumed to be inoperative. To investigate the possibility that, in fact, such excised patches retain a functional phototransduction enzymatic cascade, this same preparation was studied in darkness. Patches excised in the dark were found to retain the light sensitivity of their cGMP-induced conductance and the ability to synthesize cGMP. In the presence of guanosine 5'-[gamma-thio]triphosphate (GTP[gamma S]), a nonhydrolyzable GTP analog, light suppresses the cGMP-induced conductance irreversibly. Furthermore, inhibitors of phosphodiesterase activity reduce light sensitivity, whereas activated phosphodiesterase or activated transducin does not directly affect the channels. These results (i) establish that excised patches from rod outer segment retain functional phototransduction enzymes, (ii) support the classical view that channel opening is modulated by phosphodiesterase-mediated cGMP hydrolysis, and, most surprisingly, (iii) demonstrate that diffusion in excised patches is so restricted that local enzymes can induce variations in the concentration of small molecules. The indication that excised patches are not as simple as usually surmised opens the possibility of using them to study other intracellular transduction mechanisms.
MeSH Terms
1-Methyl-3-isobutylxanthine/pharmacology
3',5'-Cyclic-GMP Phosphodiesterases/physiology
Animals
Cell Membrane/physiology
Cyclic GMP/physiology
Electric Conductivity
Guanosine 5'-O-(3-Thiotriphosphate)
Guanosine Triphosphate/analogs & derivatives,pharmacology,physiology
Guanylate Cyclase/physiology
In Vitro Techniques
Light
Lizards
Photoreceptor Cells/physiology
Signal Transduction
Thionucleotides/pharmacology
Vision, Ocular
Chemicals
Thionucleotides
Guanosine 5'-O-(3-Thiotriphosphate)
Guanosine Triphosphate
3',5'-Cyclic-GMP Phosphodiesterases
Guanylate Cyclase
Cyclic GMP
1-Methyl-3-isobutylxanthine
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Ertel E A
Department of Physiology and Biophysics, School of Medicine, University of Washington, Seattle 98195.
References (17)
17 references, click to expand
-
Glycolysis preferentially inhibits ATP-sensitive K+ channels in isolated guinea pig cardiac myocytes.
Science. 1987 Oct 2;238(4823):67-9
PMID: 2443972
-
Regulation of cyclic GMP metabolism in toad photoreceptors. Definition of the metabolic events subserving photoexcited and attenuated states.
J Biol Chem. 1988 Jun 25;263(18):8771-85
PMID: 2837463
-
Association of guanylate cyclase with the axoneme of retinal rods.
Biochim Biophys Acta. 1980 Jun 19;630(2):176-86
PMID: 6104515
-
Direct activation of cGMP-dependent channels of retinal rods by the cGMP phosphodiesterase.
Proc Natl Acad Sci U S A. 1989 May;86(10):3634-8
PMID: 2471190
-
Regulation of cGMP-dependent conductance in cytoplasmic membrane of rod outer segments by transducin.
FEBS Lett. 1989 Apr 24;247(2):435-7
PMID: 2469603
-
Molecular mechanism of visual transduction.
Eur J Biochem. 1989 Feb 1;179(2):255-66
PMID: 2537204
-
Intracellular biochemical manipulation of phototransduction in detached rod outer segments.
Proc Natl Acad Sci U S A. 1987 Dec;84(24):9290-4
PMID: 2827176
-
Interaction of hydrolysis-resistant analogs of cyclic GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments.
Proc Natl Acad Sci U S A. 1985 Dec;82(24):8813-7
PMID: 2417228
-
Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores.
Nature. 1986 May 1-7;321(6065):70-2
PMID: 2422559
-
Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane.
Nature. 1986 May 1-7;321(6065):66-70
PMID: 2422558
-
Changes in cGMP concentration correlate with some, but not all, aspects of the light-regulated conductance of frog rod photoreceptors.
J Biol Chem. 1986 Oct 5;261(28):12965-75
PMID: 3020017
-
Light-induced losses and dark recovery rates of guanosine 3',5'-cyclic monophosphate in rod outer segments of intact amphibian photoreceptors.
J Gen Physiol. 1988 Dec;92(6):731-46
PMID: 2851028
-
Hindered diffusion in excised membrane patches from retinal rod outer segments.
Biophys J. 1988 Aug;54(2):351-5
PMID: 3207830
-
Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones.
Nature. 1985 Sep 5-11;317(6032):61-4
PMID: 2993914
-
Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment.
Nature. 1985 Jan 24-30;313(6000):310-3
PMID: 2578616
-
Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment.
Nature. 1985 Sep 19-25;317(6034):252-5
PMID: 2995816
-
Cyclic GMP cascade of vision.
Annu Rev Neurosci. 1986;9:87-119
PMID: 2423011