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Zebrafish Crb1, Localizing Uniquely to the Cell Membranes around Cone Photoreceptor Axonemes, Alleviates Light Damage to Photoreceptors and Modulates Cones' Light Responsiveness.

Authors
  • Guo, Chuanyu1
  • Deveau, Ciana2
  • Zhang, Cen1
  • Nelson, Ralph3
  • Wei, Xiangyun4, 5, 6
  • 1 Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, 15213 Pennsylvania.
  • 2 National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, 20852 Maryland.
  • 3 National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, 20852 Maryland [email protected] [email protected]
  • 4 Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, 15213 Pennsylvania [email protected] [email protected]
  • 5 Department of Molecular Genetics and Microbiology, University of Pittsburgh School of Medicine, Pittsburgh, 15213 Pennsylvania.
  • 6 Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, 15213 Pennsylvania.
Type
Published Article
Journal
Journal of Neuroscience
Publisher
Society for Neuroscience
Publication Date
Sep 09, 2020
Volume
40
Issue
37
Pages
7065–7079
Identifiers
DOI: 10.1523/JNEUROSCI.0497-20.2020
PMID: 32817065
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

The crumbs (crb) apical polarity genes are essential for the development and functions of epithelia. Adult zebrafish retinal neuroepithelium expresses three crb genes (crb1, crb2a, and crb2b); however, it is unknown whether and how Crb1 differs from other Crb proteins in expression, localization, and functions. Here, we show that, unlike zebrafish Crb2a and Crb2b as well as mammalian Crb1 and Crb2, zebrafish Crb1 does not localize to the subapical regions of photoreceptors and Müller glial cells; rather, it localizes to a small region of cone outer segments: the cell membranes surrounding the axonemes. Moreover, zebrafish Crb1 is not required for retinal morphogenesis and photoreceptor patterning. Interestingly, Crb1 promotes rod survival under strong white light irradiation in a previously unreported non--cell-autonomous fashion; in addition, Crb1 delays UV and blue cones' chromatin condensation caused by UV light irradiation. Finally, Crb1 plays a role in cones' responsiveness to light through an arrestin-translocation-independent mechanism. The localization of Crb1 and its functions do not differ between male and female fish. We conclude that zebrafish Crb1 has diverged from other vertebrate Crb proteins, representing a neofunctionalization in Crb biology during evolution.SIGNIFICANCE STATEMENT Apicobasal polarity of epithelia is an important property that underlies the morphogenesis and functions of epithelial tissues. Epithelial apicobasal polarity is controlled by many polarity genes, including the crb genes. In vertebrates, multiple crb genes have been identified, but the differences in their expression patterns and functions are not fully understood. Here, we report a novel subcellular localization of zebrafish Crb1 in retinal cone photoreceptors and evidence for its new functions in photoreceptor maintenance and light responsiveness. This study expands our understanding of the biology of the crb genes in epithelia, including retinal neuroepithelium. Copyright © 2020 the authors.

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