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Mohammad Haeri, Aphrodite Ahmadi, Barry Knox; The Flexibility of the Rod Photoreceptor Outer Segment. Invest. Ophthalmol. Vis. Sci. 2013;54(15):715.
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© ARVO (1962-2015); The Authors (2016-present)
Rod photoreceptors are modified cilia with an extended cylindrical structure specialized for phototransduction called outer segment (OS). The OS is composed of a stack of thousands of disks connected to each other via flexible linkers. High-resolution confocal/polarized microscopy shows that OS exhibits axial structural variation, with extended bands composed of a few hundred disks. The band thickness is modulated by the light condition. We investigated the role of this layered structure in the stability of the OS, which can bend or break when subjected to mechanical forces. The flexural rigidity of rods has not been explored theoretically or experimentally. In this study we investigate the stiffness of this unique layered columnar structure in photoreceptors.
We generated transgenic Xenopus expressing rhodopsin fused to eGFP under the control of Xenopus opsin promoter. Using high-resolution microscopy of live photoreceptors we recorded the OS breakage along the rod axis and its correlation to disks made in dark or light periods. We introduced a coarse-grained model of the OS mechanical rigidity using the elasticity theory. The axial OS banding was represented via a spring-bead model, and the relation for the bending stiffness of this layered structure was derived.
High-resolution confocal imaging of rods demonstrated high and low fluorescent bands generated in dark and light, respectively. The width of generated bands was proportional to the length of the dark or light period suggesting a diurnal origin. The observed fluorescent banding coincided with banding pattern recorded with DIC imaging which is similar to the banding pattern of wild type rods reported by Kaplan. Recorded images demonstrated breakage of OS in high density bands which are areas with lower flexibility. We calculated a bending stiffness of ~ 105 nN.μm2 for the OS which is 7 orders of magnitude larger than typical cilia.
Our theoretical results show that the bending stiffness has a quadratic relation to OS radius, and a direct relation to band thickness and density. Moreover, the model predicts a tendency for OS to break in bands with higher spring number density, in agreement with the experimental observation. More studies are needed to explore 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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