Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea

Buhr, Ethan D.; Yue, Wendy W.S.; Ren, Xiaozhi; Jiang, Zheng; Liao, Hsi Wen; Xue, Mei; Vemaraju, Shruti; Nguyen, My-Linh Thi; Reed, Randall R.; Lang, Richard A.; Yau, King Wai; Gelder, Russell N. Van

doi:10.1073/pnas.1516259112

Cited by 125 publications

(205 citation statements)

References 47 publications

Supporting

Mentioning

181

Contrasting

Order By: Relevance

“…PER2Luc activity of corneal tissues from control and Opn4 :: TeNT mice sacrificed at ZT8-10 were approximately antiphasic, as predicted from their circadian locomotor activity (Fig 5B and Fig 6). The lack of light entrainment of corneal tissue in the Opn4 :: TeNT mice is not consistent with previous studies showing that corneal tissue is entrained directly by light in vitro without contribution of rods, cones or ipRGCs perhaps via neuropsin signaling [46]. In the retina and cornea, light might act directly on these ocular tissues to regulate circadian phase [46, 47].…”

Section: Discussionmentioning

confidence: 58%

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

et al. 2016

View full text Add to dashboard Cite

Light is a powerful entrainer of circadian clocks in almost all eukaryotic organisms promoting synchronization of internal circadian rhythms with external environmental light-dark (LD) cycles. In mammals, the circadian system is organized in a hierarchical manner, in which a central pacemaker in the suprachiasmatic nucleus (SCN) synchronizes oscillators in peripheral tissues. Recent evidence demonstrates that photoentrainment of the SCN proceeds via signaling from a subpopulation of retinal ganglion cells (RGCs) which are melanopsin-expressing and intrinsically photosensitive (ipRGCs). However, it is still unclear whether photoentrainment of peripheral clocks is mediated exclusively by the ipRGC system or if signaling from RGCs that do not express melanopsin also plays a role. Here we have used genetic “silencing” of ipRGC neurotransmission in mice to investigate whether this photoreceptive system is obligatory for the photoentrainment of peripheral circadian clocks. Genetic silencing of ipRGC neurotransmission in mice was achieved by expression of tetanus toxin light chain in melanopsin-expressing cells (Opn4::TeNT mouse line). Rhythms of the clock gene Period 2 in various peripheral tissues were measured by crossbreeding Opn4::TeNT mice with PER2 luciferase knock-in mice (mPER2Luc). We found that in Opn4::TeNT mice the pupillary light reflex, light modulation of activity, and circadian photoentrainment of locomotor activity were severely impaired. Furthermore, ex vivo cultures from Opn4::TeNT, mPER2Luc mice of the adrenal gland, cornea, lung, liver, pituitary and spleen exhibited robust circadian rhythms of PER2::LUC bioluminescence. However, their peak bioluminescence rhythms were not aligned to the projected LD cycles indicating their lack of photic entrainment in vivo. Finally, we found that the circadian rhythm in adrenal corticosterone in Opn4::TeNT mice, as monitored by in vivo subcutaneous microdialysis, was desynchronized from environmental LD cycles. Our findings reveal a non-redundant role of ipRGCs for photic entrainment of peripheral tissues, highlighting the importance of this photoreceptive system for the organismal adaptation to daily environmental LD cycles.

show abstract

Section: Discussionmentioning

confidence: 58%

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Indeed, we demonstrate here a previously unsuspected role for light-evoked experience in the regulation of dendrite outgrowth, as evidenced by the changes in the number of melanopsin ORDs observed in DD animals. We cannot rule out the possibility that light may act via additional mechanisms to influence cone photoreceptor positioning during development, including but not limited to Opn5 /neuropsin-mediated photosensitivity (Buhr et al, 2015), or secondary effects of ipRGC silencing/light deprivation, such as altered retinal wave properties (Chew et al, 2017; Renna et al, 2011). …”

Section: Discussionmentioning

confidence: 99%

Melanopsin Retinal Ganglion Cells Regulate Cone Photoreceptor Lamination in the Mouse Retina

et al. 2018

View full text Add to dashboard Cite

SUMMARY Newborn neurons follow molecular cues to reach their final destination, but whether early life experience influences lamination remains largely unexplored. As light is among the first stimuli to reach the developing nervous system via intrinsically photosensitive retinal ganglion cells (ipRGCs), we asked whether ipRGCs could affect lamination in the developing mouse retina. We show here that ablation of ipRGCs causes cone photoreceptors to mislocalize at different apicobasal positions in the retina. This effect is partly mediated by light-evoked activity in ipRGCs, as dark rearing or silencing of ipRGCs leads a subset of cones to mislocalize. Furthermore, ablation of ipRGCs alters the cone transcriptome and decreases expression of the dopamine receptor D4, while injection of L-DOPA or D4 receptor agonist rescues the displaced cone phenotype observed in dark-reared animals. These results show that early light-mediated activity in ipRGCs influences neuronal lamination and identify ipRGC-elicited dopamine release as a mechanism influencing cone position.

show abstract

“…Finally, the enigmatic neuropsins (NEUR in Fig. 2A) from the Group 4 opsin clade form UVS visual pigments and are expressed in a variety of vertebrate neuronal tissues, including retinal ganglion cells and the pineal body (Buhr et al, 2015;Yamashita et al, 2010). The function of neuropsin is poorly understood, but it appears to play a role in circadian entrainment in some cases.…”

Section: Uv Visual Pigmentsmentioning

confidence: 99%

Photoreception and vision in the ultraviolet

Cronin

Bok

2016

Journal of Experimental Biology

145

128

View full text Add to dashboard Cite

Ultraviolet (UV) light occupies the spectral range of wavelengths slightly shorter than those visible to humans. Because of its shorter wavelength, it is more energetic (and potentially more photodamaging) than 'visible light', and it is scattered more efficiently in air and water. Until 1990, only a few animals were recognized as being sensitive to UV light, but we now know that a great diversity, possibly even the majority, of animal species can visually detect and respond to it. Here, we discuss the history of research on biological UV photosensitivity and review current major research trends in this field. Some animals use their UV photoreceptors to control simple, innate behaviors, but most incorporate their UV receptors into their general sense of vision. They not only detect UV light but recognize it as a separate color in light fields, on natural objects or living organisms, or in signals displayed by conspecifics. UV visual pigments are based on opsins, the same family of proteins that are used to detect light in conventional photoreceptors. Despite some interesting exceptions, most animal species have a single photoreceptor class devoted to the UV. The roles of UV in vision are manifold, from guiding navigation and orientation behavior, to detecting food and potential predators, to supporting high-level tasks such as mate assessment and intraspecific communication. Our current understanding of UV vision is restricted almost entirely to two phyla: arthropods and chordates (specifically, vertebrates), so there is much comparative work to be done.

show abstract

Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea

Cited by 125 publications

References 47 publications

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

Intrinsically Photosensitive Retinal Ganglion Cells (ipRGCs) Are Necessary for Light Entrainment of Peripheral Clocks

Melanopsin Retinal Ganglion Cells Regulate Cone Photoreceptor Lamination in the Mouse Retina

Photoreception and vision in the ultraviolet

Contact Info

Product

Resources

About