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

Overview

Journal J Neurosci

Specialty Neurology

Date 2020 Aug 21

PMID 32817065

Citations 3

Authors

Chuanyu Guo

Ciana Deveau

Cen Zhang

Ralph Nelson

Xiangyun Wei

Affiliations

Soon will be listed here.

Abstract

The () apical polarity genes are essential for the development and functions of epithelia. Adult zebrafish retinal neuroepithelium expresses three genes (, , and ); 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. 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 genes. In vertebrates, multiple 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 genes in epithelia, including retinal neuroepithelium.

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References

Pan D . The hippo signaling pathway in development and cancer. Dev Cell. 2010; 19(4):491-505. PMC: 3124840. DOI: 10.1016/j.devcel.2010.09.011. View

Jacobson S, Cideciyan A, Aleman T, Pianta M, Sumaroka A, Schwartz S . Crumbs homolog 1 (CRB1) mutations result in a thick human retina with abnormal lamination. Hum Mol Genet. 2003; 12(9):1073-8. DOI: 10.1093/hmg/ddg117. View

Vallespin E, Cantalapiedra D, Riveiro-Alvarez R, Wilke R, Aguirre-Lamban J, Avila-Fernandez A . Mutation screening of 299 Spanish families with retinal dystrophies by Leber congenital amaurosis genotyping microarray. Invest Ophthalmol Vis Sci. 2007; 48(12):5653-61. DOI: 10.1167/iovs.07-0007. View

Lessieur E, Fogerty J, Gaivin R, Song P, Perkins B . The Ciliopathy Gene ahi1 Is Required for Zebrafish Cone Photoreceptor Outer Segment Morphogenesis and Survival. Invest Ophthalmol Vis Sci. 2017; 58(1):448-460. PMC: 5270624. DOI: 10.1167/iovs.16-20326. View

Thomas J, Thummel R . A novel light damage paradigm for use in retinal regeneration studies in adult zebrafish. J Vis Exp. 2013; (80):e51017. PMC: 3960977. DOI: 10.3791/51017. View

Konieczny A, Ausubel F . A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993; 4(2):403-10. DOI: 10.1046/j.1365-313x.1993.04020403.x. View

Thomas J, Nelson C, Luo X, Hyde D, Thummel R . Characterization of multiple light damage paradigms reveals regional differences in photoreceptor loss. Exp Eye Res. 2012; 97(1):105-16. PMC: 3329775. DOI: 10.1016/j.exer.2012.02.004. View

Chen C, Gajewski K, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C . The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci U S A. 2010; 107(36):15810-5. PMC: 2936591. DOI: 10.1073/pnas.1004060107. View

Tepass U . Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila. Dev Biol. 1996; 177(1):217-25. DOI: 10.1006/dbio.1996.0157. View

10.

den Hollander A, Ten Brink J, de Kok Y, Van Soest S, van den Born L, van Driel M . Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet. 1999; 23(2):217-21. DOI: 10.1038/13848. View

11.

Pocha S, Wassmer T, Niehage C, Hoflack B, Knust E . Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr Biol. 2011; 21(13):1111-7. DOI: 10.1016/j.cub.2011.05.007. View

12.

Nam S, Choi K . Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development. 2003; 130(18):4363-72. DOI: 10.1242/dev.00648. View

13.

Tepass U, Theres C, Knust E . crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell. 1990; 61(5):787-99. DOI: 10.1016/0092-8674(90)90189-l. View

14.

Pocha S, Shevchenko A, Knust E . Crumbs regulates rhodopsin transport by interacting with and stabilizing myosin V. J Cell Biol. 2011; 195(5):827-38. PMC: 3257572. DOI: 10.1083/jcb.201105144. View

15.

Wei X, Zou J, Takechi M, Kawamura S, Li L . Nok plays an essential role in maintaining the integrity of the outer nuclear layer in the zebrafish retina. Exp Eye Res. 2006; 83(1):31-44. PMC: 2923805. DOI: 10.1016/j.exer.2005.10.030. View

16.

Chartier F, Hardy E, Laprise P . Crumbs limits oxidase-dependent signaling to maintain epithelial integrity and prevent photoreceptor cell death. J Cell Biol. 2012; 198(6):991-8. PMC: 3444775. DOI: 10.1083/jcb.201203083. View

17.

Bulgakova N, Knust E . The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J Cell Sci. 2009; 122(Pt 15):2587-96. DOI: 10.1242/jcs.023648. View

18.

Alves C, Pellissier L, Wijnholds J . The CRB1 and adherens junction complex proteins in retinal development and maintenance. Prog Retin Eye Res. 2014; 40:35-52. DOI: 10.1016/j.preteyeres.2014.01.001. View

19.

Parsons L, Grzeschik N, Allott M, Richardson H . Lgl/aPKC and Crb regulate the Salvador/Warts/Hippo pathway. Fly (Austin). 2010; 4(4):288-93. PMC: 3174480. DOI: 10.4161/fly.4.4.13116. View

20.

Letizia A, Ricardo S, Moussian B, Martin N, Llimargas M . A functional role of the extracellular domain of Crumbs in cell architecture and apicobasal polarity. J Cell Sci. 2013; 126(Pt 10):2157-63. DOI: 10.1242/jcs.122382. View