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

The molecular circadian clocks in the mammalian retina are locally synchronized by environmental light cycles independent of the suprachiasmatic nuclei (SCN) in the brain. Unexpectedly, this entrainment does not require rods, cones, or melanopsin (OPN4), possibly suggesting the involvement of anothe...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 112; no. 42; pp. 13093 - 13098
Main Authors Buhr, Ethan D., Yue, Wendy W. S., Ren, Xiaozhi, Jiang, Zheng, Liao, Hsi-Wen Rock, Mei, Xue, Vemaraju, Shruti, Nguyen, Minh-Thanh, Reed, Randall R., Lang, Richard A., Yau, King-Wai, Van Gelder, Russell N.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 20.10.2015
National Acad Sciences
Subjects
Animals
Biological Sciences
Brain
Circadian rhythm
Cornea
Cornea - physiology
Membrane Proteins - genetics
Membrane Proteins - physiology
Mice
Mice, Knockout
Opsins - genetics
Opsins - physiology
Retina
Retina - physiology
Rodents
Suprachiasmatic Nucleus - physiology
Ultraviolet Rays
photoentrainment
cornea
retina
OPN5
circadian rhythm
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Summary:The molecular circadian clocks in the mammalian retina are locally synchronized by environmental light cycles independent of the suprachiasmatic nuclei (SCN) in the brain. Unexpectedly, this entrainment does not require rods, cones, or melanopsin (OPN4), possibly suggesting the involvement of another retinal photopigment. Here, we show that the ex vivo mouse retinal rhythm is most sensitive to short-wavelength light but that this photoentrainment requires neither the short-wavelength–sensitive cone pigment [S-pigment or cone opsin (OPN1SW)] nor encephalopsin (OPN3). However, retinas lacking neuropsin (OPN5) fail to photoentrain, even though other visual functions appear largely normal. Initial evidence suggests that OPN5 is expressed in select retinal ganglion cells. Remarkably, the mouse corneal circadian rhythm is also photoentrainable ex vivo, and this photoentrainment likewise requires OPN5. Our findings reveal a light-sensing function for mammalian OPN5, until now an orphan opsin.
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Reviewers: C.B.G., University of Texas Southwestern Medical Center; and C.P.R., University of Texas Health Science Center at Houston.
1Present address: Department of Neurobiology, Harvard Medical School, Boston, MA 02115.
Contributed by King-Wai Yau, August 17, 2015 (sent for review July 22, 2015; reviewed by Carla B. Green and Christophe P. Ribelayga)
Author contributions: E.D.B. and R.N.V.G. designed and performed all photoentrainment experiments; H.-W.R.L. made the Opn5−/− line 1; W.W.S.Y. characterized the Opn5−/− line 1; X.R. generated the Opn3−/− mouse line; W.W.S.Y. performed the X-Gal labelings (Opn5−/− line 1) and immunolabelings (line 1); S.V. performed the X-Gal labelings (line 2); W.W.S.Y. and Z.J. performed the CMFDG labeling and subsequent injection of Alexa dyes (line 1); R.R.R. provided invaluable advice on molecular biology and genetics; X.M., S.V., M.-T.N., and R.A.L generated and characterized the Opn5−/− line 2; and E.D.B., W.W.S.Y., R.A.L., K.-W.Y., and R.N.V.G wrote the paper.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1516259112