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Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure

The first steps of vision take place within a stack of tightly packed disc-shaped membranes, or ‘discs’, located in the outer segment compartment of photoreceptor cells. In rod photoreceptors, discs are enclosed inside the outer segment and contain deep indentations in their rims called ‘incisures’....

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Autores principales: Lewis, Tylor R, Phan, Sebastien, Castillo, Carson M, Kim, Keun-Young, Coppenrath, Kelsey, Thomas, William, Hao, Ying, Skiba, Nikolai P, Horb, Marko E, Ellisman, Mark H, Arshavsky, Vadim Y
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10361718/
https://www.ncbi.nlm.nih.gov/pubmed/37449984
http://dx.doi.org/10.7554/eLife.89160
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author Lewis, Tylor R
Phan, Sebastien
Castillo, Carson M
Kim, Keun-Young
Coppenrath, Kelsey
Thomas, William
Hao, Ying
Skiba, Nikolai P
Horb, Marko E
Ellisman, Mark H
Arshavsky, Vadim Y
author_facet Lewis, Tylor R
Phan, Sebastien
Castillo, Carson M
Kim, Keun-Young
Coppenrath, Kelsey
Thomas, William
Hao, Ying
Skiba, Nikolai P
Horb, Marko E
Ellisman, Mark H
Arshavsky, Vadim Y
author_sort Lewis, Tylor R
collection PubMed
description The first steps of vision take place within a stack of tightly packed disc-shaped membranes, or ‘discs’, located in the outer segment compartment of photoreceptor cells. In rod photoreceptors, discs are enclosed inside the outer segment and contain deep indentations in their rims called ‘incisures’. The presence of incisures has been documented in a variety of species, yet their role remains elusive. In this study, we combined traditional electron microscopy with three-dimensional electron tomography to demonstrate that incisures are formed only after discs become completely enclosed. We also observed that, at the earliest stage of their formation, discs are not round as typically depicted but rather are highly irregular in shape and resemble expanding lamellipodia. Using genetically manipulated mice and frogs and measuring outer segment protein abundances by quantitative mass spectrometry, we further found that incisure size is determined by the molar ratio between peripherin-2, a disc rim protein critical for the process of disc enclosure, and rhodopsin, the major structural component of disc membranes. While a high perpherin-2 to rhodopsin ratio causes an increase in incisure size and structural complexity, a low ratio precludes incisure formation. Based on these data, we propose a model whereby normal rods express a modest excess of peripherin-2 over the amount required for complete disc enclosure in order to ensure that this important step of disc formation is accomplished. Once the disc is enclosed, the excess peripherin-2 incorporates into the rim to form an incisure.
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spelling pubmed-103617182023-07-22 Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure Lewis, Tylor R Phan, Sebastien Castillo, Carson M Kim, Keun-Young Coppenrath, Kelsey Thomas, William Hao, Ying Skiba, Nikolai P Horb, Marko E Ellisman, Mark H Arshavsky, Vadim Y eLife Cell Biology The first steps of vision take place within a stack of tightly packed disc-shaped membranes, or ‘discs’, located in the outer segment compartment of photoreceptor cells. In rod photoreceptors, discs are enclosed inside the outer segment and contain deep indentations in their rims called ‘incisures’. The presence of incisures has been documented in a variety of species, yet their role remains elusive. In this study, we combined traditional electron microscopy with three-dimensional electron tomography to demonstrate that incisures are formed only after discs become completely enclosed. We also observed that, at the earliest stage of their formation, discs are not round as typically depicted but rather are highly irregular in shape and resemble expanding lamellipodia. Using genetically manipulated mice and frogs and measuring outer segment protein abundances by quantitative mass spectrometry, we further found that incisure size is determined by the molar ratio between peripherin-2, a disc rim protein critical for the process of disc enclosure, and rhodopsin, the major structural component of disc membranes. While a high perpherin-2 to rhodopsin ratio causes an increase in incisure size and structural complexity, a low ratio precludes incisure formation. Based on these data, we propose a model whereby normal rods express a modest excess of peripherin-2 over the amount required for complete disc enclosure in order to ensure that this important step of disc formation is accomplished. Once the disc is enclosed, the excess peripherin-2 incorporates into the rim to form an incisure. eLife Sciences Publications, Ltd 2023-07-14 /pmc/articles/PMC10361718/ /pubmed/37449984 http://dx.doi.org/10.7554/eLife.89160 Text en © 2023, Lewis et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Lewis, Tylor R
Phan, Sebastien
Castillo, Carson M
Kim, Keun-Young
Coppenrath, Kelsey
Thomas, William
Hao, Ying
Skiba, Nikolai P
Horb, Marko E
Ellisman, Mark H
Arshavsky, Vadim Y
Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title_full Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title_fullStr Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title_full_unstemmed Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title_short Photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
title_sort photoreceptor disc incisures form as an adaptive mechanism ensuring the completion of disc enclosure
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10361718/
https://www.ncbi.nlm.nih.gov/pubmed/37449984
http://dx.doi.org/10.7554/eLife.89160
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