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      Morphological and physiological characteristics of dermal photoreceptors in Lymnaea stagnalis

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          Abstract

          Dermal photoreceptors located in the mantle of Lymnaea stagnalis were histologically and physiologically characterized. Our previous study demonstrated that the shadow response from dermal photoreceptors induces the whole-body withdrawal response. Through the interneuron, RPeD11, we detected that the light-off response indirectly originated from a dermal photoreceptor. Previous observations, based on behavioral pharmacology, revealed that cyclic guanosine monophosphate acts as a second messenger in the dermal photoreceptor. Furthermore, gastropods possess dermal photoreceptors containing rhodopsin, as a photopigment, and another photo-sensitive protein, arrestin, responsible for terminating the light response. Thus, we chose three antibodies, anti-cGMP, anti-rhodopsin, and anti-β-arrestin, to identify the dermal photoreceptor molecules in Lymnaea mantle. Extracellular recording, using a suction electrode on the mantle, revealed a light off-response from the right parietal nerve. Overlapping structures, positive against each of the antibodies, were also observed. Numerous round, granular particles of 3–47 μm in diameter with one nucleus were distributed around pneumostome and/or inside the mantle. The cells surrounding the pneumostome area, located 10 μm beneath the surface, tended to have smaller cell soma ranging from 3 to 25 μm in diameter, while cells located in other areas were distributed uniformly inside the mantle, with a larger diameter ranging from 12 to 47 μm. The histological examination using back-filing Lucifer Yellow staining of the right parietal nerve with the three dermal photoreceptor antibodies confirmed that these overlapping-stained structures were dermal photoreceptors in Lymnaea.

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          Most cited references42

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          Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions.

          In rod photoreceptors, arrestin localizes to the outer segment (OS) in the light and to the inner segment (IS) in the dark. Here, we demonstrate that redistribution of arrestin between these compartments can proceed in ATP-depleted photoreceptors. Translocation of transducin from the IS to the OS also does not require energy, but depletion of ATP or GTP inhibits its reverse movement. A sustained presence of activated rhodopsin is required for sequestering arrestin in the OS, and the rate of arrestin relocalization to the OS is determined by the amount and the phosphorylation status of photolyzed rhodopsin. Interaction of arrestin with microtubules is increased in the dark. Mutations that enhance arrestin-microtubule binding attenuate arrestin translocation to the OS. These results indicate that the distribution of arrestin in rods is controlled by its dynamic interactions with rhodopsin in the OS and microtubules in the IS and that its movement occurs by simple diffusion.
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            The history of the Drosophila TRP channel: the birth of a new channel superfamily.

            Transient receptor potential (TRP) channels are polymodal cellular sensors involved in a wide variety of cellular processes, mainly by changing membrane voltage and increasing cellular Ca(2+). This review outlines in detail the history of the founding member of the TRP family, the Drosophila TRP channel. The field began with a spontaneous mutation in the trp gene that led to a blind mutant during prolonged intense light. It was this mutant that allowed for the discovery of the first TRP channels. A combination of electrophysiological, biochemical, Ca(2+) measurements, and genetic studies in flies and in other invertebrates pointed to TRP as a novel phosphoinositide-regulated and Ca(2+)-permeable channel. The cloning and sequencing of the trp gene provided its molecular identity. These seminal findings led to the isolation of the first mammalian homologues of the Drosophila TRP channels. We now know that TRP channel proteins are conserved through evolution and are found in most organisms, tissues, and cell-types. The TRP channel superfamily is classified into seven related subfamilies: TRPC, TRPM, TRPV, TRPA, TRPP, TRPML, and TRPN. A great deal is known today about participation of TRP channels in many biological processes, including initiation of pain, thermoregulation, salivary fluid secretion, inflammation, cardiovascular regulation, smooth muscle tone, pressure regulation, Ca(2+) and Mg(2+) homeostasis, and lysosomal function. The native Drosophila photoreceptor cells, where the founding member of the TRP channels superfamily was found, is still a useful preparation to study basic features of this remarkable channel.
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              Visual arrestins in olfactory pathways of Drosophila and the malaria vector mosquito Anopheles gambiae.

              Arrestins are important components for desensitization of G protein-coupled receptor cascades that mediate neurotransmission as well as olfactory and visual sensory reception. We have isolated AgArr1, an arrestin-encoding cDNA from the malaria vector mosquito, Anopheles gambiae, where olfaction is critical for vectorial capacity. Analysis of AgArr1 expression revealed an overlap between chemosensory and photoreceptor neurons. Furthermore, an examination of previously identified arrestins from Drosophila melanogaster exposed similar bimodal expression, and Drosophila arrestin mutants demonstrate impaired electrophysiological responses to olfactory stimuli. Thus, we show that arrestins in Drosophila are required for normal olfactory physiology in addition to their previously described role in visual signaling. These findings suggest that individual arrestins function in both olfactory and visual pathways in Dipteran insects; these genes may prove useful in the design of control strategies that target olfactory-dependent behaviors of insect disease vectors.
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                Author and article information

                Journal
                Biophysics (Nagoya-shi)
                Biophysics (Nagoya-shi)
                biop
                Biophysics
                The Biophysical Society of Japan (BSJ)
                1349-2942
                2014
                11 November 2014
                : 10
                : 77-88
                Affiliations
                [1 ]Graduate School of High-Technology for Human Welfare, Tokai University, Numazu, Shizuoka 410-0321, Japan
                [2 ]Graduate School of Bioscience, Tokai University, Numazu, Shizuoka 410-0321, Japan
                [3 ]Hotchkiss Brain Institute, Faculty of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada
                [4 ]School of Engineering, Department of Biomedical Engineering, Tokai University, Hiratsuka, Kanagawa 259-1292, Japan
                [5 ]School of High-Technology for Human Welfare, Tokai University, Numazu, Shizuoka 410-0321, Japan
                Author notes
                Corresponding author: Manabu Sakakibara, Laboratory of Neurobiological Engineering, School of High-Technology for Human Welfare, Tokai University, Numazu, Shizuoka 410-0321, Japan. e-mail: manabu@ 123456tokai.ac.jp
                Article
                10_77
                10.2142/biophysics.10.77
                4629660
                ae63c5c4-5863-4c9c-977b-72933db6ebf3
                ©2014 THE BIOPHYSICAL SOCIETY OF JAPAN
                History
                : 05 September 2014
                : 14 October 2014
                Categories
                Regular Article

                immunohistochemistry,electrophysiology,extracellular recording,rhodopsin,cgmp,β arrestin

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