Changes in cGMP concentration correlate with some, but not all, aspects of the light-regulated conductance of frog rod photoreceptors

R. H. Cote, Grant Nicol, S. A. Burke, M. D. Bownds

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Cyclic GMP has been implicated in controlling the light-regulated conductance of rod photorecptors of the vertebrate retina. However, there is little direct evidence correlating changes in cGMP concentration with the light-regulated permeability mechanism in living cells. A preparation of intact frog rod outer segments suspended in a Ringer's medium containing low Ca2+ has been used to demonstrate that initial changes in total cellular cGMP concentration parallel changes in the light-regulated membrane current over a wide range of light intensities. At light intensities bleaching from 160 to 5.6 x 106 rhodopsin molecules/rod/s, decreases in the response latency for the cGMP kinetics parallel decreases in the latent period of the electrical response. Further, changes in the rate of the cGMP decrease parallel the rate of membrane current suppression as the light intensity is varied. Up to 105 cGMP molecules are hydrolyzed per photolyzed rhodopsin, consistent with in vitro studies showing that each bleached rhodopsin can activate over 100 phosphodiesterase molecules. Addition of the Ca2+ ionophore, A23187, does not affect the initial kinetics of the cGMP decrease or of the electrical response, excluding a direct role for Ca2+ in the initial events of phototransduction. These results are consistent with cGMP being the intracellular messenger that links rhodopsin isomerization with changes in membrane permeability upon illumination. It is unlikely, however, that light-induced changes in total cGMP concentration are the sole regulators of membrane current. This is suggested by several observations: 1) at bright light intensities, the subsecond light-induced cGMP decrease is essentially complete prior to complete suppression of membrane current; 2) maximal light-induced decreases in cGMP concentration occur at all light intensities tested, whereas the extent of membrane current suppression varies over the same range of light intensities; 3) changing the external Ca2+ concentration from 1 mM to 10 nM in the dark causes an increase in membrane current that is significantly more rapid than corresponding changes in cGMP concentration. Thus, light-induced changes in total cellular cGMP concentration correlate with some, but not all, aspects of the visual excitation process in vertebrate photoreceptors.

Original languageEnglish (US)
Pages (from-to)12965-12975
Number of pages11
JournalJournal of Biological Chemistry
Volume261
Issue number28
StatePublished - 1986
Externally publishedYes

Fingerprint

Retinal Rod Photoreceptor Cells
Anura
Light
Rhodopsin
Membranes
Molecules
Permeability
Light Signal Transduction
Rod Cell Outer Segment
Vertebrate Photoreceptor Cells
Kinetics
Ionophores
Cyclic GMP
Phosphoric Diester Hydrolases
Calcimycin
Bleaching
Isomerization
Lighting
Reaction Time
Vertebrates

ASJC Scopus subject areas

  • Biochemistry

Cite this

Changes in cGMP concentration correlate with some, but not all, aspects of the light-regulated conductance of frog rod photoreceptors. / Cote, R. H.; Nicol, Grant; Burke, S. A.; Bownds, M. D.

In: Journal of Biological Chemistry, Vol. 261, No. 28, 1986, p. 12965-12975.

Research output: Contribution to journalArticle

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abstract = "Cyclic GMP has been implicated in controlling the light-regulated conductance of rod photorecptors of the vertebrate retina. However, there is little direct evidence correlating changes in cGMP concentration with the light-regulated permeability mechanism in living cells. A preparation of intact frog rod outer segments suspended in a Ringer's medium containing low Ca2+ has been used to demonstrate that initial changes in total cellular cGMP concentration parallel changes in the light-regulated membrane current over a wide range of light intensities. At light intensities bleaching from 160 to 5.6 x 106 rhodopsin molecules/rod/s, decreases in the response latency for the cGMP kinetics parallel decreases in the latent period of the electrical response. Further, changes in the rate of the cGMP decrease parallel the rate of membrane current suppression as the light intensity is varied. Up to 105 cGMP molecules are hydrolyzed per photolyzed rhodopsin, consistent with in vitro studies showing that each bleached rhodopsin can activate over 100 phosphodiesterase molecules. Addition of the Ca2+ ionophore, A23187, does not affect the initial kinetics of the cGMP decrease or of the electrical response, excluding a direct role for Ca2+ in the initial events of phototransduction. These results are consistent with cGMP being the intracellular messenger that links rhodopsin isomerization with changes in membrane permeability upon illumination. It is unlikely, however, that light-induced changes in total cGMP concentration are the sole regulators of membrane current. This is suggested by several observations: 1) at bright light intensities, the subsecond light-induced cGMP decrease is essentially complete prior to complete suppression of membrane current; 2) maximal light-induced decreases in cGMP concentration occur at all light intensities tested, whereas the extent of membrane current suppression varies over the same range of light intensities; 3) changing the external Ca2+ concentration from 1 mM to 10 nM in the dark causes an increase in membrane current that is significantly more rapid than corresponding changes in cGMP concentration. Thus, light-induced changes in total cellular cGMP concentration correlate with some, but not all, aspects of the visual excitation process in vertebrate photoreceptors.",
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