title: Calcium-independent, cGMP-mediated light adaptation in invertebrate ciliary photoreceptors.
abstract: Calcium is thought to be essential for adaptation of sensory receptor cells. However, the transduction cascade of hyperpolarizing, ciliary photoreceptors of the scallop does not use IP3-mediated Ca release, and the light-sensitive conductance is not measurably permeable to Ca2+. Therefore, two typical mechanisms that couple the light response to [Ca]i changes seem to be lacking in these photoreceptors. Using fluorescent indicators, we determined that, unlike in their microvillar counterparts, photostimulation of ciliary cells under voltage clamp indeed evokes no detectable change in cytosolic Ca. Notwithstanding, these cells exhibit all of the hallmarks of light adaptation, including response range compression, sensitivity shift, and photoresponse acceleration. A possible mediator of Ca-independent sensory adaptation is cGMP, the second messenger that regulates the light-sensitive conductance; cGMP and 8-bromo cGMP not only activate light-dependent K channels but also reduce the amplitude of the light response to an extent greatly in excess of that expected from simple occlusion between light and chemical stimulation. In addition, these substances accelerate the time course of the photocurrent. Tests with pharmacological antagonists suggest that protein kinase G may be a downstream effector that controls, in part, the cGMP-triggered changes in photoresponse properties during light adaptation. However, additional messengers are likely to be implicated, especially in the regulation of response kinetics. These observations suggest a novel feedback inhibition pathway for signaling sensory adaptation.
authors.affiliation: Department of Physiology and Biophysics, Boston University School of Medicine, Boston, Massachusetts 02118, USA. mpgomez@bu.edu
authors.forename: Maria
authors.initials: M
authors.lastname: del Pilar Gomez
authors.forename: Enrico
authors.initials: E
authors.lastname: Nasi
mesh_terms: D000222:Adaptation, Physiological / Q000502:physiology*; D000818:Animals; D002118:Calcium / Q000032:analysis / Q000502:physiology*; D002227:Carbazoles / Q000494:pharmacology; D002923:Cilia / Q000528:radiation effects*; D006152:Cyclic GMP / Q000031:analogs & derivatives / Q000494:pharmacology / Q000502:physiology*; D017869:Cyclic GMP-Dependent Protein Kinases / Q000037:antagonists & inhibitors; D025461:Feedback, Physiological / Q000502:physiology*; D007211:Indoles / Q000494:pharmacology; D008974:Mollusca / Q000502:physiology / Q000528:radiation effects*; D018408:Patch-Clamp Techniques; D010775:Photic Stimulation; D017956:Photoreceptor Cells, Invertebrate / Q000502:physiology / Q000528:radiation effects*; D047428:Protein Kinase Inhibitors / Q000494:pharmacology; D015290:Second Messenger Systems / Q000502:physiology*
chemical_list: D002227:Carbazoles; D007211:Indoles; D047428:Protein Kinase Inhibitors; C073601:KT 5823; C016276:8-bromocyclic GMP; D017869:Cyclic GMP-Dependent Protein Kinases; D006152:Cyclic GMP; D002118:Calcium
references.citation: J Gen Physiol. 1999 Nov;114(5):653-72
references.pmid: 10532963
references.citation: J Neurosci. 2000 Jul 15;20(14):5254-63
references.pmid: 10884309
references.citation: Physiol Rev. 2001 Jan;81(1):117-151
references.pmid: 11152756
references.citation: J Physiol. 2002 Sep 1;543(Pt 2):481-94
references.pmid: 12205183
references.citation: Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):471-4
references.pmid: 1370581
references.citation: Science. 1991 Dec 6;254(5037):1478-84
references.pmid: 1962207
references.citation: Nature. 1986 Jul 17-23;322(6076):261-3
references.pmid: 21898960
references.citation: Neuron. 1990 Apr;4(4):547-55
references.pmid: 2322460
references.citation: J Neurosci. 1988 Sep;8(9):3240-6
references.pmid: 2459322
references.citation: Nature. 1985 Feb 14-20;313(6003):579-82
references.pmid: 2578628
references.citation: J Gen Physiol. 1986 Feb;87(2):243-69
references.pmid: 3081681
references.citation: J Gen Physiol. 1986 Jul;88(1):107-26
references.pmid: 3734748
references.citation: J Gen Physiol. 1974 Dec;64(6):643-65
references.pmid: 4155426
references.citation: J Physiol. 1979 Jun;291:207-232
references.pmid: 480206
references.citation: J Gen Physiol. 1972 Jun;59(6):701-19
references.pmid: 5025746
references.citation: J Gen Physiol. 1977 Nov;70(5):591-600
references.pmid: 591913
references.citation: Cell Mol Neurobiol. 1983 Dec;3(4):311-28
references.pmid: 6325009
references.citation: J Physiol. 1978 Feb;275:345-55
references.pmid: 633125
references.citation: Nature. 1984 May 24-30;309(5966):352-4
references.pmid: 6427629
references.citation: Nature. 1984 Oct 18-24;311(5987):661-3
references.pmid: 6434995
references.citation: Anal Biochem. 1983 Nov;135(1):112-9
references.pmid: 6670734
references.citation: Physiol Rev. 1995 Oct;75(4):725-48
references.pmid: 7480160
references.citation: J Neurosci. 1995 Jan;15(1 Pt 2):889-902
references.pmid: 7529832
references.citation: Neuron. 1995 Sep;15(3):607-18
references.pmid: 7546740
references.citation: J Gen Physiol. 1994 Jun;103(6):939-56
references.pmid: 7931139
references.citation: J Gen Physiol. 1975 Oct;66(4):489-506
references.pmid: 810540
references.citation: J Gen Physiol. 1976 Apr;67(4):475-91
references.pmid: 818341
references.citation: Nature. 1993 Jun 17;363(6430):634-7
references.pmid: 8510756
references.citation: Neuron. 1996 Aug;17(2):323-31
references.pmid: 8780655
references.citation: J Neurochem. 1997 Feb;68(2):443-56
references.pmid: 9003029
references.citation: J Gen Physiol. 1997 Mar;109(3):371-84
references.pmid: 9089443
references.citation: J Biol Chem. 1997 Sep 12;272(37):22979-82
references.pmid: 9287291