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An opsin 5-dopamine pathway mediates light-dependent vascular development in the eye.

ABSTRACT: During mouse postnatal eye development, the embryonic hyaloid vascular network regresses from the vitreous as an adaption for high-acuity vision. This process occurs with precisely controlled timing. Here, we show that opsin 5 (OPN5; also known as neuropsin)-dependent retinal light responses regulate vascular development in the postnatal eye. In Opn5-null mice, hyaloid vessels regress precociously. We demonstrate that 380-nm light stimulation via OPN5 and VGAT (the vesicular GABA/glycine transporter) in retinal ganglion cells enhances the activity of inner retinal DAT (also known as SLC6A3; a dopamine reuptake transporter) and thus suppresses vitreal dopamine. In turn, dopamine acts directly on hyaloid vascular endothelial cells to suppress the activity of vascular endothelial growth factor receptor 2 (VEGFR2) and promote hyaloid vessel regression. With OPN5 loss of function, the vitreous dopamine level is elevated and results in premature hyaloid regression. These investigations identify violet light as a developmental timing cue that, via an OPN5-dopamine pathway, regulates optic axis clearance in preparation for visual function.

SUBMITTER: Nguyen MT

PROVIDER: S-EPMC6573021 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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An opsin 5-dopamine pathway mediates light-dependent vascular development in the eye.

Nguyen Minh-Thanh T MT Vemaraju Shruti S Nayak Gowri G Odaka Yoshinobu Y Buhr Ethan D ED Alonzo Nuria N Tran Uyen U Batie Matthew M Upton Brian A BA Darvas Martin M Kozmik Zbynek Z Rao Sujata S Hegde Rashmi S RS Iuvone P Michael PM Van Gelder Russell N RN Lang Richard A RA

Nature cell biology 20190401 4

During mouse postnatal eye development, the embryonic hyaloid vascular network regresses from the vitreous as an adaption for high-acuity vision. This process occurs with precisely controlled timing. Here, we show that opsin 5 (OPN5; also known as neuropsin)-dependent retinal light responses regulate vascular development in the postnatal eye. In Opn5-null mice, hyaloid vessels regress precociously. We demonstrate that 380-nm light stimulation via OPN5 and VGAT (the vesicular GABA/glycine transpo ...[more]

PMID: 30936473

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Project description:BackgroundAnimals living in well-lit environments utilize optical stimuli for detecting visual information, regulating the homeostatic pacemaker, and controlling patterns of body pigmentation. In contrast, many subterranean animal species without optical stimuli have evolved regressed binocular eyes and body pigmentation. Interestingly, some fossorial and cave-dwelling animals with regressed eyes still respond to light. These light-dependent responses may be simply evolutionary residuals or they may be adaptive, where negative phototaxis provides avoidance of predator-rich surface environments. However, the relationship between these non-ocular light responses and the underlying light-sensing Opsin proteins has not been fully elucidated.MethodsTo highlight the potential functions of opsins in a blind subterranean animal, we used the Mexican cave tetra to investigate opsin gene expression in the eyes and several brain regions of both surface and cave-dwelling adults. We performed database surveys, expression analyses by quantitative reverse transcription PCR (RT-qPCR), and light-dependent locomotor activity analysis using pinealectomized fish, one of the high-opsin expressing organs of cavefish.ResultsBased on conservative criteria, we identified 33 opsin genes in the cavefish genome. Surveys of available RNAseq data found 26 of these expressed in the surface fish eye as compared to 24 expressed in cavefish extraocular tissues, 20 of which were expressed in the brain. RT-qPCR of 26 opsins in surface and cavefish eye and brain tissues showed the highest opsin-expressing tissue in cavefish was the pineal organ, which expressed exo-rhodopsin at 72.7% of the expression levels in surface fish pineal. However, a pinealectomy resulted in no change to the light-dependent locomotor activity in juvenile cavefish and surface fish. Therefore, we conclude that, after 20,000 or more years of evolution in darkness, cavefish light-dependent basal activity is regulated by a non-pineal extraocular organ.

Dataset Information

An opsin 5-dopamine pathway mediates light-dependent vascular development in the eye.

Publications

An opsin 5-dopamine pathway mediates light-dependent vascular development in the eye.

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