A novel Ca2+-feedback mechanism extends the operating range of mammalian rods to brighter light
Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual p...
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Published in | The Journal of general physiology Vol. 146; no. 4; pp. 307 - 321 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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United States
The Rockefeller University Press
01.10.2015
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Abstract | Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual photons, but remain responsive to visual stimuli under conditions of bright ambient light, which would be expected to saturate their response given the high gain of the rod transduction cascade in darkness. These photoreceptors regulate their sensitivity to light rapidly and reversibly in response to changes in ambient illumination, thereby avoiding saturation. Calcium ions (Ca2+) play a major role in mediating the rapid, subsecond adaptation to light, and the Ca2+-binding proteins GCAP1 and GCAP2 (or guanylyl cyclase-activating proteins [GCAPs]) have been identified as important mediators of the photoreceptor response to changes in intracellular Ca2+. However, mouse rods lacking both GCAP1 and GCAP2 (GCAP-/-) still show substantial light adaptation. Here, we determined the Ca2+ dependency of this residual light adaptation and, by combining pharmacological, genetic, and electrophysiological tools, showed that an unknown Ca2+-dependent mechanism contributes to light adaptation in GCAP-/- mouse rods. We found that mimicking the light-induced decrease in intracellular [Ca2+] accelerated recovery of the response to visual stimuli and caused a fourfold decrease of sensitivity in GCAP-/- rods. About half of this Ca2+-dependent regulation of sensitivity could be attributed to the recoverin-mediated pathway, whereas half of it was caused by the unknown mechanism. Furthermore, our data demonstrate that the feedback mechanisms regulating the sensitivity of mammalian rods on the second and subsecond time scales are all Ca2+ dependent and that, unlike salamander rods, Ca2+-independent background-induced acceleration of flash response kinetics is rather weak in mouse rods. |
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AbstractList | Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual photons, but remain responsive to visual stimuli under conditions of bright ambient light, which would be expected to saturate their response given the high gain of the rod transduction cascade in darkness. These photoreceptors regulate their sensitivity to light rapidly and reversibly in response to changes in ambient illumination, thereby avoiding saturation. Calcium ions (Ca2+) play a major role in mediating the rapid, subsecond adaptation to light, and the Ca2+-binding proteins GCAP1 and GCAP2 (or guanylyl cyclase–activating proteins [GCAPs]) have been identified as important mediators of the photoreceptor response to changes in intracellular Ca2+. However, mouse rods lacking both GCAP1 and GCAP2 (GCAP−/−) still show substantial light adaptation. Here, we determined the Ca2+ dependency of this residual light adaptation and, by combining pharmacological, genetic, and electrophysiological tools, showed that an unknown Ca2+-dependent mechanism contributes to light adaptation in GCAP−/− mouse rods. We found that mimicking the light-induced decrease in intracellular [Ca2+] accelerated recovery of the response to visual stimuli and caused a fourfold decrease of sensitivity in GCAP−/− rods. About half of this Ca2+-dependent regulation of sensitivity could be attributed to the recoverin-mediated pathway, whereas half of it was caused by the unknown mechanism. Furthermore, our data demonstrate that the feedback mechanisms regulating the sensitivity of mammalian rods on the second and subsecond time scales are all Ca2+ dependent and that, unlike salamander rods, Ca2+-independent background-induced acceleration of flash response kinetics is rather weak in mouse rods. A previously unidentified calcium-dependent mechanism contributes to light adaptation in mammalian rods. Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual photons, but remain responsive to visual stimuli under conditions of bright ambient light, which would be expected to saturate their response given the high gain of the rod transduction cascade in darkness. These photoreceptors regulate their sensitivity to light rapidly and reversibly in response to changes in ambient illumination, thereby avoiding saturation. Calcium ions (Ca 2+ ) play a major role in mediating the rapid, subsecond adaptation to light, and the Ca 2+ -binding proteins GCAP1 and GCAP2 (or guanylyl cyclase–activating proteins [GCAPs]) have been identified as important mediators of the photoreceptor response to changes in intracellular Ca 2+ . However, mouse rods lacking both GCAP1 and GCAP2 (GCAP −/− ) still show substantial light adaptation. Here, we determined the Ca 2+ dependency of this residual light adaptation and, by combining pharmacological, genetic, and electrophysiological tools, showed that an unknown Ca 2+ -dependent mechanism contributes to light adaptation in GCAP −/− mouse rods. We found that mimicking the light-induced decrease in intracellular [Ca 2+ ] accelerated recovery of the response to visual stimuli and caused a fourfold decrease of sensitivity in GCAP −/− rods. About half of this Ca 2+ -dependent regulation of sensitivity could be attributed to the recoverin-mediated pathway, whereas half of it was caused by the unknown mechanism. Furthermore, our data demonstrate that the feedback mechanisms regulating the sensitivity of mammalian rods on the second and subsecond time scales are all Ca 2+ dependent and that, unlike salamander rods, Ca 2+ -independent background-induced acceleration of flash response kinetics is rather weak in mouse rods. Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the range over which they operate. For instance, rod photoreceptors are extremely sensitive in darkness, so that they are able to detect individual photons, but remain responsive to visual stimuli under conditions of bright ambient light, which would be expected to saturate their response given the high gain of the rod transduction cascade in darkness. These photoreceptors regulate their sensitivity to light rapidly and reversibly in response to changes in ambient illumination, thereby avoiding saturation. Calcium ions (Ca2+) play a major role in mediating the rapid, subsecond adaptation to light, and the Ca2+-binding proteins GCAP1 and GCAP2 (or guanylyl cyclase-activating proteins [GCAPs]) have been identified as important mediators of the photoreceptor response to changes in intracellular Ca2+. However, mouse rods lacking both GCAP1 and GCAP2 (GCAP-/-) still show substantial light adaptation. Here, we determined the Ca2+ dependency of this residual light adaptation and, by combining pharmacological, genetic, and electrophysiological tools, showed that an unknown Ca2+-dependent mechanism contributes to light adaptation in GCAP-/- mouse rods. We found that mimicking the light-induced decrease in intracellular [Ca2+] accelerated recovery of the response to visual stimuli and caused a fourfold decrease of sensitivity in GCAP-/- rods. About half of this Ca2+-dependent regulation of sensitivity could be attributed to the recoverin-mediated pathway, whereas half of it was caused by the unknown mechanism. Furthermore, our data demonstrate that the feedback mechanisms regulating the sensitivity of mammalian rods on the second and subsecond time scales are all Ca2+ dependent and that, unlike salamander rods, Ca2+-independent background-induced acceleration of flash response kinetics is rather weak in mouse rods. |
Author | Turunen, Teemu T Pitkänen, Marja Vinberg, Frans Koskelainen, Ari Heikkinen, Hanna |
AuthorAffiliation | 1 Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland 2 Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110 |
AuthorAffiliation_xml | – name: 1 Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland – name: 2 Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110 |
Author_xml | – sequence: 1 givenname: Frans surname: Vinberg fullname: Vinberg, Frans email: ari.koskelainen@aalto.fi, frans.vinberg@gmail.com organization: Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110 ari.koskelainen@aalto.fi frans.vinberg@gmail.com – sequence: 2 givenname: Teemu T surname: Turunen fullname: Turunen, Teemu T organization: Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland – sequence: 3 givenname: Hanna surname: Heikkinen fullname: Heikkinen, Hanna organization: Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland – sequence: 4 givenname: Marja surname: Pitkänen fullname: Pitkänen, Marja organization: Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland – sequence: 5 givenname: Ari surname: Koskelainen fullname: Koskelainen, Ari email: ari.koskelainen@aalto.fi, frans.vinberg@gmail.com organization: Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, FI-00076 Aalto, Finland ari.koskelainen@aalto.fi frans.vinberg@gmail.com |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26415569$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_3389_fnmol_2018_00473 crossref_primary_10_1093_hmg_ddw228 crossref_primary_10_1113_JP281225 crossref_primary_10_1038_s41598_018_34073_8 crossref_primary_10_1098_rsob_180076 crossref_primary_10_1074_jbc_RA117_001574 crossref_primary_10_1016_j_preteyeres_2021_101040 crossref_primary_10_1016_j_gep_2017_03_001 crossref_primary_10_1016_j_cub_2018_02_062 crossref_primary_10_1038_s41598_018_37661_w crossref_primary_10_1016_j_jbc_2021_101401 crossref_primary_10_1038_s41598_021_88140_8 |
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Snippet | Sensory cells adjust their sensitivity to incoming signals, such as odor or light, in response to changes in background stimulation, thereby extending the... A previously unidentified calcium-dependent mechanism contributes to light adaptation in mammalian rods. Sensory cells adjust their sensitivity to incoming... |
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SubjectTerms | Animals Calcium Signaling Cells, Cultured Feedback, Physiological Guanylate Cyclase-Activating Proteins - genetics Guanylate Cyclase-Activating Proteins - metabolism Mice Mice, Inbred C57BL Retinal Rod Photoreceptor Cells - metabolism |
Title | A novel Ca2+-feedback mechanism extends the operating range of mammalian rods to brighter light |
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