Structural interpretation of the birefringence gradient in retinal rod outer segments

Corless, Joseph M.; Kaplan, Michael W.

doi:10.1016/s0006-3495(79)85270-4

Cited by 18 publications

(8 citation statements)

References 19 publications

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“…Earlier detection of “birefringence bands” using polarized light microscopy has suggested that the structure of the disc membranes along the axis of the frog OS is not uniform (Corless and Kaplan, 1979). The periodic birefringence band pattern can also be disrupted when the frogs are maintained in either constant dark or constant light (Kaplan, 1981).…”

Section: Discussionmentioning

confidence: 99%

Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors

2015

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The outer segment (OS) of the rod photoreceptor is a light-sensing cilium containing ∼1,000 membrane-bound discs. Each day, discs constituting the distal tenth of the OS are shed, while nascent discs are formed at the base of the OS through the incorporation of molecules transported from the inner segment. The mechanisms regulating these processes remain elusive. Here we show that rhodopsin preferentially enters the OS in the dark. Photoexcitation of post-Golgi rhodopsins retains them in the inner segment. Disc-rim protein peripherin2/rds enters the OS following a rhythm complementary to that of rhodopsin. Light-dark cycle-regulated protein trafficking serves as a mechanism to segregate rhodopsin-rich and peripherin2/rds-rich discs into alternating stacks, which are flanked by characteristic cytoplasmic pockets. This periodic cytostructure divides the OS into ∼10 fractions, each containing discs synthesized in a single day. This mechanism may explain how the rod photoreceptor balances the quantity of discs added and removed daily.

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Section: Discussionmentioning

confidence: 99%

Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors

2015

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“…There appears to be a structural feature that extends across many OS disks. This was originally observed in frogs as an axial inhomogeneity of the OS under polarized light, as alternating dark and bright birefringence bands in isolated and fixed amphibian rod OS (18)(19)(20)(21)(22)(23), and was first reported by Kaplan (20). This feature has been subsequently found in many species including rat, guinea pig, rabbit, dog, and monkey (19,20,24).…”

Section: Introductionmentioning

confidence: 86%

Modeling the Flexural Rigidity of Rod Photoreceptors

Haeri

Knox

Ahmadi

2013

Biophysical Journal

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In vertebrate eyes, the rod photoreceptor has a modified cilium with an extended cylindrical structure specialized for phototransduction called the outer segment (OS). The OS has numerous stacked membrane disks and can bend or break when subjected to mechanical forces. The OS exhibits axial structural variation, with extended bands composed of a few hundred membrane disks whose thickness is diurnally modulated. Using high-resolution confocal microscopy, we have observed OS flexing and disruption in live transgenic Xenopus rods. Based on the experimental observations, we introduce a coarse-grained model of OS mechanical rigidity using elasticity theory, representing the axial OS banding explicitly via a spring-bead model. We calculate a bending stiffness of ∼10(5) nN⋅μm2, which is seven orders-of-magnitude larger than that of typical cilia and flagella. This bending stiffness has a quadratic relation to OS radius, so that thinner OS have lower fragility. Furthermore, we find that increasing the spatial frequency of axial OS banding decreases OS rigidity, reducing its fragility. Moreover, the model predicts a tendency for OS to break in bands with higher spring number density, analogous to the experimental observation that transgenic rods tended to break preferentially in bands of high fluorescence. We discuss how pathological alterations of disk membrane properties by mutant proteins may lead to increased OS rigidity and thus increased breakage, ultimately contributing to retinal degeneration.

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“…In the dark-adapted rod the exceptionally high refractive indexes of the IS and OS (33) certainly exceed those of the extracellular matrix and RPE near the OS tips. Calculations based on well-known dielectric mixing models (58)(59)(60) predict that 10% elongation of the rod OS will cause the average refractive index of the OS to decrease (Model of the Light-Induced Backscatter Increase from the OS and Fig. S4).…”

Section: Estimating the Spring Constant Of An Elementary Rod Os Elasticmentioning

confidence: 99%

In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors

Zhang

Zawadzki

Goswami

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

115

164

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The light responses of rod and cone photoreceptors have been studied electrophysiologically for decades, largely with ex vivo approaches that disrupt the photoreceptors' subretinal microenvironment. Here we report the use of optical coherence tomography (OCT) to measure light-driven signals of rod photoreceptors in vivo. Visible light stimulation over a 200-fold intensity range caused correlated rod outer segment (OS) elongation and increased light scattering in wildtype mice, but not in mice lacking the rod G-protein alpha subunit, transducin (Gα t ), revealing these responses to be triggered by phototransduction. For stimuli that photoactivated one rhodopsin per Gα t the rod OS swelling response reached a saturated elongation of 10.0 ± 2.1%, at a maximum rate of 0.11% s −1. Analyzing swelling as osmotically driven water influx, we find the H 2 O membrane permeability of the rod OS to be (2.6 ± 0.4) × 10 −5 cm·s, comparable to that of other cells lacking aquaporin expression. Application of Van't Hoff's law reveals that complete activation of phototransduction generates a potentially harmful 20% increase in OS osmotic pressure. The increased backscattering from the base of the OS is explained by a model combining cytoplasmic swelling, translocation of dissociated G-protein subunits from the disc membranes into the cytoplasm, and a relatively higher H 2 O permeability of nascent discs in the basal rod OS. Translocation of phototransduction components out of the OS may protect rods from osmotic stress, which could be especially harmful in disease conditions that affect rod OS structural integrity.osmotic stress | phototransduction | optical coherence tomography | intrinsic optical signals | photoreceptor waveguiding

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Structural interpretation of the birefringence gradient in retinal rod outer segments

Cited by 18 publications

References 19 publications

Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors

Light Regulates the Ciliary Protein Transport and Outer Segment Disc Renewal of Mammalian Photoreceptors

Modeling the Flexural Rigidity of Rod Photoreceptors

In vivo optophysiology reveals that G-protein activation triggers osmotic swelling and increased light scattering of rod photoreceptors

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