Super-resolution mapping in rod photoreceptors identifies rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway

Super-resolution mapping in rod photoreceptors identifies rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway

Photoreceptor cells in the vertebrate retina have a highly compartmentalized morphology for efficient phototransduction and vision. Rhodopsin, the visual pigment in rod photoreceptors, is densely packaged into the rod outer segment sensory cilium and continuously renewed through essential synthesis...

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Published in:PLoS biology Vol. 22; no. 1; p. e3002467
Main Authors: Haggerty, Kristen N, Eshelman, Shannon C, Sexton, Lauren A, Frimpong, Emmanuel, Rogers, Leah M, Agosto, Melina A, Robichaux, Michael A
Format: Journal Article
Language:English
Published: United States Public Library of Science 08-01-2024
Public Library of Science (PLoS)
Subjects:
Analysis
Animals
Biology and Life Sciences
Cell Membrane
Cell membranes
Cytology
Fluorescence microscopy
Homeostasis
Labeling
Light Signal Transduction
Localization
Mammals
Medicine and Health Sciences
Membranes
Mice
Microscopy
Microscopy, Fluorescence
Monoclonal antibodies
Mutation
Photopigments
Photoreception
Photoreceptors
Phototransduction
Plasma
Proteins
Research and Analysis Methods
Retina
Retinal Rod Photoreceptor Cells
Rhodopsin
Rod outer segment membranes
Segments
Social Sciences
Vertebrates
Visual pigments
Canada
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Abstract Photoreceptor cells in the vertebrate retina have a highly compartmentalized morphology for efficient phototransduction and vision. Rhodopsin, the visual pigment in rod photoreceptors, is densely packaged into the rod outer segment sensory cilium and continuously renewed through essential synthesis and trafficking pathways housed in the rod inner segment. Despite the importance of this region for rod health and maintenance, the subcellular organization of rhodopsin and its trafficking regulators in the mammalian rod inner segment remain undefined. We used super-resolution fluorescence microscopy with optimized retinal immunolabeling techniques to perform a single molecule localization analysis of rhodopsin in the inner segments of mouse rods. We found that a significant fraction of rhodopsin molecules was localized at the plasma membrane, at the surface, in an even distribution along the entire length of the inner segment, where markers of transport vesicles also colocalized. Thus, our results collectively establish a model of rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway in mouse rod photoreceptors.
AbstractList Photoreceptor cells in the vertebrate retina have a highly compartmentalized morphology for efficient phototransduction and vision. Rhodopsin, the visual pigment in rod photoreceptors, is densely packaged into the rod outer segment sensory cilium and continuously renewed through essential synthesis and trafficking pathways housed in the rod inner segment. Despite the importance of this region for rod health and maintenance, the subcellular organization of rhodopsin and its trafficking regulators in the mammalian rod inner segment remain undefined. We used super-resolution fluorescence microscopy with optimized retinal immunolabeling techniques to perform a single molecule localization analysis of rhodopsin in the inner segments of mouse rods. We found that a significant fraction of rhodopsin molecules was localized at the plasma membrane, at the surface, in an even distribution along the entire length of the inner segment, where markers of transport vesicles also colocalized. Thus, our results collectively establish a model of rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway in mouse rod photoreceptors.
Photoreceptor cells in the vertebrate retina have a highly compartmentalized morphology for efficient phototransduction and vision. Rhodopsin, the visual pigment in rod photoreceptors, is densely packaged into the rod outer segment sensory cilium and continuously renewed through essential synthesis and trafficking pathways housed in the rod inner segment. Despite the importance of this region for rod health and maintenance, the subcellular organization of rhodopsin and its trafficking regulators in the mammalian rod inner segment remain undefined. We used super-resolution fluorescence microscopy with optimized retinal immunolabeling techniques to perform a single molecule localization analysis of rhodopsin in the inner segments of mouse rods. We found that a significant fraction of rhodopsin molecules was localized at the plasma membrane, at the surface, in an even distribution along the entire length of the inner segment, where markers of transport vesicles also colocalized. Thus, our results collectively establish a model of rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway in mouse rod photoreceptors. Photoreceptor cells of the retina are maintained through a complex protein trafficking network. This study uses quantitative super-resolution microscopy to reveal the trafficking of the essential visual pigment rhodopsin in the inner segment region of rod photoreceptors.
Audience Academic
Author Sexton, Lauren A
Agosto, Melina A
Rogers, Leah M
Robichaux, Michael A
Haggerty, Kristen N
Eshelman, Shannon C
Frimpong, Emmanuel
AuthorAffiliation 2 Retina and Optic Nerve Research Laboratory, Department of Physiology and Biophysics, and Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, Nova Scotia, Canada
University of Sussex, UNITED KINGDOM
1 Department of Ophthalmology & Visual Sciences and Department of Biochemistry & Molecular Medicine, West Virginia University, Morgantown, West Virginia, United States of America
AuthorAffiliation_xml – name: 2 Retina and Optic Nerve Research Laboratory, Department of Physiology and Biophysics, and Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, Nova Scotia, Canada
– name: University of Sussex, UNITED KINGDOM
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  givenname: Kristen N
  surname: Haggerty
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  organization: Department of Ophthalmology & Visual Sciences and Department of Biochemistry & Molecular Medicine, West Virginia University, Morgantown, West Virginia, United States of America
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  givenname: Shannon C
  orcidid: 0000-0003-2357-1466
  surname: Eshelman
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  givenname: Lauren A
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  fullname: Rogers, Leah M
  organization: Department of Ophthalmology & Visual Sciences and Department of Biochemistry & Molecular Medicine, West Virginia University, Morgantown, West Virginia, United States of America
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  givenname: Melina A
  orcidid: 0000-0002-3647-1926
  surname: Agosto
  fullname: Agosto, Melina A
  organization: Retina and Optic Nerve Research Laboratory, Department of Physiology and Biophysics, and Department of Ophthalmology and Visual Sciences, Dalhousie University, Halifax, Nova Scotia, Canada
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  givenname: Michael A
  orcidid: 0000-0002-2559-4912
  surname: Robichaux
  fullname: Robichaux, Michael A
  organization: Department of Ophthalmology & Visual Sciences and Department of Biochemistry & Molecular Medicine, West Virginia University, Morgantown, West Virginia, United States of America
BackLink https://www.ncbi.nlm.nih.gov/pubmed/38190419$$D View this record in MEDLINE/PubMed
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2024 Haggerty et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet Photoreceptor cells in the vertebrate retina have a highly compartmentalized morphology for efficient phototransduction and vision. Rhodopsin, the visual...
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StartPage e3002467
SubjectTerms Analysis
Animals
Biology and Life Sciences
Cell Membrane
Cell membranes
Cytology
Fluorescence microscopy
Homeostasis
Labeling
Light Signal Transduction
Localization
Mammals
Medicine and Health Sciences
Membranes
Mice
Microscopy
Microscopy, Fluorescence
Monoclonal antibodies
Mutation
Photopigments
Photoreception
Photoreceptors
Phototransduction
Plasma
Proteins
Research and Analysis Methods
Retina
Retinal Rod Photoreceptor Cells
Rhodopsin
Rod outer segment membranes
Segments
Social Sciences
Vertebrates
Visual pigments
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Title Super-resolution mapping in rod photoreceptors identifies rhodopsin trafficking through the inner segment plasma membrane as an essential subcellular pathway
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