Rhodopsin Expression Level Affects Rod Outer Segment Morphology and Photoresponse Kinetics

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Rhodopsin Expression Level Affects Rod Outer Segment Morphology and Photoresponse Kinetics

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dc.contributor.author Michaud, Norman A.
dc.contributor.author Covington, Henry I.
dc.contributor.author DiBenedetto, Emmanuele
dc.contributor.author Hamm, Heidi E.
dc.contributor.author Lem, Janis
dc.contributor.author Caruso, Giovanni
dc.contributor.author Makino, Clint L.
dc.contributor.author Wen, Xiao-Hong
dc.date.accessioned 2013-03-14T18:24:34Z
dc.date.issued 2012
dc.identifier.citation Makino, Clint L., Xiao-Hong Wen, Norman A. Michaud, Henry I. Covington, Emmanuele DiBenedetto, Heidi E. Hamm, Janis Lem, and Giovanni Caruso. 2012. Rhodopsin expression level affects rod outer segment morphology and photoresponse kinetics. PLoS ONE 7(5): e37832. en_US
dc.identifier.issn 1932-6203 en_US
dc.identifier.uri http://nrs.harvard.edu/urn-3:HUL.InstRepos:10406318
dc.description.abstract Background: The retinal rod outer segment is a sensory cilium that is specialized for the conversion of light into an electrical signal. Within the cilium, up to several thousand membranous disks contain as many as a billion copies of rhodopsin for efficient photon capture. Disks are continually turned over, requiring the daily synthesis of a prodigious amount of rhodopsin. To promote axial diffusion in the aqueous cytoplasm, the disks have one or more incisures. Across vertebrates, the range of disk diameters spans an order of magnitude, and the number and length of the incisures vary considerably, but the mechanisms controlling disk architecture are not well understood. The finding that transgenic mice overexpressing rhodopsin have enlarged disks lacking an incisure prompted us to test whether lowered rhodopsin levels constrain disk assembly. Methodology/Principal Findings: The structure and function of rods from hemizygous rhodopsin knockout (R+/−) mice with decreased rhodopsin expression were analyzed by transmission electron microscopy and single cell recording. R+/− rods were structurally altered in three ways: disk shape changed from circular to elliptical, disk surface area decreased, and the single incisure lengthened to divide the disk into two sections. Photocurrent responses to flashes recovered more rapidly than normal. A spatially resolved model of phototransduction indicated that changes in the packing densities of rhodopsin and other transduction proteins were responsible. The decrease in aqueous outer segment volume and the lengthened incisure had only minor effects on photon response amplitude and kinetics. Conclusions/Significance: Rhodopsin availability limits disk assembly and outer segment girth in normal rods. The incisure may buffer the supply of structural proteins needed to form larger disks. Decreased rhodopsin level accelerated photoresponse kinetics by increasing the rates of molecular collisions on the membrane. Faster responses, together with fewer rhodopsins, combine to lower overall sensitivity of R+/− rods to light. en_US
dc.language.iso en_US en_US
dc.publisher Public Library of Science en_US
dc.relation.isversionof doi:10.1371/journal.pone.0037832 en_US
dc.relation.hasversion http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3360601/pdf/ en_US
dash.license LAA
dc.subject Biology en_US
dc.subject Anatomy and Physiology en_US
dc.subject Neurological System en_US
dc.subject Sensory Physiology en_US
dc.subject Biochemistry en_US
dc.subject Cytochemistry en_US
dc.subject Cell Membrane en_US
dc.subject Membrane Proteins en_US
dc.subject Membrane Structures en_US
dc.subject Organelles en_US
dc.subject Neuroscience en_US
dc.subject Cellular Neuroscience en_US
dc.subject Neuronal Morphology en_US
dc.subject Sensory Systems en_US
dc.subject Visual System en_US
dc.title Rhodopsin Expression Level Affects Rod Outer Segment Morphology and Photoresponse Kinetics en_US
dc.type Journal Article en_US
dc.description.version Version of Record en_US
dc.relation.journal PLoS ONE en_US
dash.depositing.author Makino, Clint L.
dc.date.available 2013-03-14T18:24:34Z

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