Skip to main content
SpringerLink
Log in

Light entrainment of retinal biorhythms: cryptochrome 2 as candidate photoreceptor in mammals

  • Visions and reflections
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The mechanisms that synchronize the biorhythms of the mammalian retina with the light/dark cycle are independent of those synchronizing the rhythms in the central pacemaker, the suprachiasmatic nucleus. The identity of the photoreceptor(s) responsible for the light entrainment of the retina of mammals is still a matter of debate, and recent studies have reported contradictory results in this respect. Here, we suggest that cryptochromes (CRY), in particular CRY 2, are involved in that light entrainment. CRY are highly conserved proteins that are a key component of the cellular circadian clock machinery. In plants and insects, they are responsible for the light entrainment of these biorhythms, mediated by the light response of their flavin cofactor (FAD). In mammals, however, no light-dependent role is currently assumed for CRY in light-exposed tissues, including the retina. It has been reported that FAD influences the function of mammalian CRY 2 and that human CRY 2 responds to light in Drosophila, suggesting that mammalian CRY 2 keeps the ability to respond to light. Here, we hypothesize that CRY 2 plays a role in the light entrainment of retinal biorhythms, at least in diurnal mammals. Indeed, published data shows that the light intensity dependence and the wavelength sensitivity commonly reported for that light entrainment fits the light sensitivity and absorption spectrum of light-responsive CRY. We propose experiments to test our hypothesis and to further explore the still-pending question of the function of CRY 2 in the mammalian retina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Astiz M, Heyde I, Oster H (2019) Mechanisms of communication in the mammalian circadian timing system. Int J Mol Sci 20:E343. https://doi.org/10.3390/ijms20020343

    Article  CAS  PubMed  Google Scholar 

  2. Husse J, Eichele G, Oster H (2015) Synchronization of the mammalian circadian timing system: light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body’s circadian clock network with external time. BioEssays 37:1119–1128. https://doi.org/10.1002/bies.201500026

    Article  PubMed  PubMed Central  Google Scholar 

  3. Welz PS, Zinna VM, Symeonidi A, Koronowski KB, Kinouchi K, Smith JG, Guillén IM, Castellanos A, Furrow S, Aragón F, Crainiciuc G, Prats N, Caballero JM, Hidalgo A, Sassone-Corsi P, Benitah SA (2019) BMAL1-driven tissue clocks respond independently to light to maintain homeostasis. Cell 177:1436–1447. https://doi.org/10.1016/j.cell.2019.05.009

    Article  CAS  PubMed  Google Scholar 

  4. Fan SM, Chang YT, Chen CL, Wang WH, Pan MK, Chen WP, Huang WY, Xu Z, Huang HE, Chen T, Plikus MV, Chen SK, Lin SJ (2018) External light activates hair follicle stem cells through eyes via an ipRGC-SCN-sympathetic neural pathway. Proc Natl Acad Sci USA 115:E6880–E6889. https://doi.org/10.1073/pnas.1719548115

    Article  CAS  PubMed  Google Scholar 

  5. Buhr ED, Vemaraju S, Diaz N, Lang RA, Van Gelder RN (2019) Neuropsin (OPN5) mediates local light-dependent induction of circadian clock genes and circadian photoentrainment in exposed murine skin. Curr Biol 29:1–10. https://doi.org/10.1016/j.cub.2019.08.063

    Article  CAS  Google Scholar 

  6. Tosini G, Menaker M (1996) Circadian rhythms in cultured mammal retina. Science 272:419–421. https://doi.org/10.1126/science.272.5260.419

    Article  CAS  PubMed  Google Scholar 

  7. Owens L, Buhr ED, Tu DC, Lamprecht TL, Lee J, Van Gelder RN (2012) Effect of circadian clock gene mutations on nonvisual photoreception in the mouse. Investig Ophthalmol Vis Sci 53:454–460. https://doi.org/10.1167/iovs.11-8717

    Article  CAS  Google Scholar 

  8. Buhr ED, Van Gelder RN (2014) Local photic entrainment of the retinal circadian oscillator in the absence of rods, cones, and melanopsin. Proc Natl Acad Sci USA 111:8625–8630. https://doi.org/10.1073/pnas.1323350111

    Article  CAS  PubMed  Google Scholar 

  9. Felder-Schmittbuhl MP, Buhr ED, Dkhissi-Benyahya O, Hicks D, Peirson SN, Ribelayga CP, Sandu C, Spessert R, Tosini G (2018) Ocular clocks: adapting mechanisms for eye functions and health. Investig Ophthalmol Vis Sci 59:4856–4870. https://doi.org/10.1167/iovs.18-24957

    Article  CAS  Google Scholar 

  10. Tosini G, Menaker M (1998) The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain Res 789:221–228. https://doi.org/10.1016/s0006-8993(97)01446-7

    Article  CAS  PubMed  Google Scholar 

  11. Buhr ED, Yue WW, Ren X, Jiang Z, Liao HW, Mei X, Vemaraju S, Nguyen MT, Reed RR, Lang RA, Yau KW, Van Gelder RN (2015) Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea. Proc Natl Acad Sci USA 112:13093–13098. https://doi.org/10.1073/pnas.1516259112

    Article  CAS  PubMed  Google Scholar 

  12. Calligaro H, Coutanson C, Najjar RP, Mazzaro N, Cooper HM, Haddjeri N, Felder-Schmittbuhl MP, Dkhissi-Benyahya O (2019) Rods contribute to the light-induced phase shift of the retinal clock in mammals. PLoS Biol 17:e2006211. https://doi.org/10.1371/journal.pbio.2006211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ruan GX, Allen GC, Yamazaki S, McMahon DG (2008) An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol 6:e249. https://doi.org/10.1371/journal.pbio.0060249

    Article  CAS  PubMed  Google Scholar 

  14. Peirson SN, Brown LA, Pothecary CA, Benson LA, Fisk AS (2018) Light and the laboratory mouse. J Neurosci Methods 15(300):26–36. https://doi.org/10.1016/j.jneumeth.2017.04.007

    Article  Google Scholar 

  15. Brown TM (2016) Using light to tell the time of day: sensory coding in the mammalian circadian visual network. J Exp Biol 219(Pt 12):1779–1792. https://doi.org/10.1242/jeb.132167

    Article  PubMed  PubMed Central  Google Scholar 

  16. Haltaufderhyde K, Ozdeslik RN, Wicks NL, Najera JA, Oancea E (2015) Opsin expression in human epidermal skin. Photochem Photobiol 91:117–123. https://doi.org/10.1111/php.12354

    Article  CAS  PubMed  Google Scholar 

  17. Spitschan M (2019) Melanopsin contribution to non-visual and visual function. Curr Opin Behav Sci 30:67–72. https://doi.org/10.1016/j.cobeha.2019.06.004

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kojima D, Mori S, Torii M, Wada A, Morishita R, Fukada Y (2011) UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS One 6:e26388. https://doi.org/10.1371/journal.pone.0026388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Liu H, Zhong D, Lin C (2010) Searching for a photocycle of the cryptochrome photoreceptors. Curr Opin Plant Biol 13:578–586. https://doi.org/10.1016/j.pbi.2010.09.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hut RA, Scheper A, Daan S (2000) Can the circadian system of a diurnal and a nocturnal rodent entrain to ultraviolet light ? J Comp Physiol A 186:707–715

    Article  CAS  Google Scholar 

  21. Mure LS, Le HD, Benegiamo G, Chang MW, Rios L, Jillani N, Ngotho M, Kariuki T, Dkhissi-Benyahya O, Cooper HM, Panda S (2018) Diurnal transcriptome atlas of a primate across major neural and peripheral tissues. Science 359:eaao0318. https://doi.org/10.1126/science.aao0318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lall GS, Revell VL, Momiji H, Al Enezi J, Altimus CM, Güler AD, Aguilar C, Cameron MA, Allender S, Hankins MW, Lucas RJ (2010) Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 66:417–428. https://doi.org/10.1016/j.neuron.2010.04.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Oztürk N, Song SH, Ozgür S, Selby CP, Morrison L, Partch C, Zhong D, Sancar A (2007) Structure and function of animal cryptochromes. Cold Spring Harb Symp Quant Biol 72:119–131. https://doi.org/10.1101/sqb.2007.72.015

    Article  PubMed  Google Scholar 

  24. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364. https://doi.org/10.1146/annurev-arplant-042110-103759

    Article  CAS  PubMed  Google Scholar 

  25. Czarna A, Berndt A, Singh HR, Grudziecki A, Ladurner AG, Timinszky G, Kramer A, Wolf E (2013) Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function. Cell 153:1394–1405. https://doi.org/10.1016/j.cell.2013.05.011

    Article  CAS  PubMed  Google Scholar 

  26. Zoltowski BD, Chelliah Y, Wickramaratne A, Jarocha L, Karki N, Xu W, Mouritsen H, Hore PJ, Hibbs RE, Green CB, Takahashi JS (2019) Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1907875116

    Article  PubMed  Google Scholar 

  27. Liu Q, Wang Q, Deng W, Wang X, Piao M, Cai D, Li Y, Barshop WD, Yu X, Zhou T, Liu B, Oka Y, Wohlschlegel J, Zuo Z, Lin C (2017) Molecular basis for blue light-dependent phosphorylation of Arabidopsis cryptochrome 2. Nat Commun 8:15234. https://doi.org/10.1038/ncomms15234

    Article  PubMed  PubMed Central  Google Scholar 

  28. Weidler G, Zur Oven-Krockhaus S, Heunemann M, Orth C, Schleifenbaum F, Harter K, Hoecker U, Batschauer A (2012) Degradation of Arabidopsis CRY2 is regulated by SPA proteins and phytochrome A. Plant Cell 24:2610–2623. https://doi.org/10.1105/tpc.112.098210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gustafson CL, Partch CL (2015) Emerging models for the molecular basis of mammalian circadian timing. Biochemistry 54:134–149. https://doi.org/10.1021/bi500731f

    Article  CAS  PubMed  Google Scholar 

  30. Wong JCY, Smyllie NJ, Banks GT, Pothecary CA, Barnard AR, Maywood ES, Jagannath A, Hughes S, van der Horst GTJ, MacLaren RE, Hankins MW, Hastings MH, Nolan PM, Foster RG, Peirson SN (2018) Differential roles for cryptochromes in the mammalian retinal clock. FASEB J 32:4302–4314. https://doi.org/10.1096/fj.201701165RR

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Thompson CL, Bowes Rickman C, Shaw SJ, Kelly U, Sancar A, Rickman DW (2003) Expression of the blue-light receptor cryptochrome in the human retina. Investig Ophthalmol Vis Sci 44:4515–4521. https://doi.org/10.1167/iovs.03-0303

    Article  Google Scholar 

  32. Wang X, Jing C, Selby CP, Chiou YY, Yang Y, Wu W, Sancar A, Wang J (2018) Comparative properties and functions of type 2 and type 4 pigeon cryptochromes. Cell Mol Life Sci 75:4629–4641. https://doi.org/10.1007/s00018-018-2920-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Partch CL, Sancar A (2005) Cryptochromes and circadian photoreception in animals. Methods Enzymol 393:726–745. https://doi.org/10.1016/S0076-6879(05)93038-3

    Article  CAS  PubMed  Google Scholar 

  34. Van Gelder RN, Wee R, Lee JA, Tu DC (2003) Reduced pupillary light responses in mice lacking cryptochromes. Science 299:222. https://doi.org/10.1126/science.1079536

    Article  PubMed  Google Scholar 

  35. Hore PJ, Mouritsen H (2016) The radical-pair mechanism of magnetoreception. Annu Rev Biophys 45:299–344. https://doi.org/10.1146/annurev-biophys-032116-094545

    Article  CAS  PubMed  Google Scholar 

  36. Kattnig DR, Evans EW, Déjean V, Dodson CA, Wallace MI, Mackenzie SR, Timmel CR, Hore PJ (2016) Chemical amplification of magnetic field effects relevant to avian magnetoreception. Nat Chem 8:384–391. https://doi.org/10.1038/nchem.2447

    Article  CAS  PubMed  Google Scholar 

  37. Sheppard DM, Li J, Henbest KB, Neil SR, Maeda K, Storey J, Schleicher E, Biskup T, Rodriguez R, Weber S, Hore PJ, Timmel CR, Mackenzie SR (2017) Millitesla magnetic field effects on the photocycle of an animal cryptochrome. Sci Rep 7:42228. https://doi.org/10.1038/srep42228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Günther A, Einwich A, Sjulstock E, Feederlee R, Bolte P, Koch KW, Solov’yov IA, Mouritsen H (2018) Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4. Curr Biol 28:211–223. https://doi.org/10.1016/j.cub.2017.12.003

    Article  CAS  PubMed  Google Scholar 

  39. Begall S, Malkemper EP, Ceverny J, Nemec P, Burda H (2013) Magnetic alignment in mammals and other animals. Mammal Biol 78:10–20. https://doi.org/10.1016/j.mambio.2012.05.005

    Article  Google Scholar 

  40. Begall S, Burda H, Malkemper EP (2014) Magnetoreception in mammals. In: Naguib M (ed) Advances in the study of behavior, vol 46. Elsevier, Amsterdam, pp 45–88. https://doi.org/10.1016/B978-0-12-800286-5.00002-X

    Google Scholar 

  41. Hirano A, Braas D, Fu YH, Ptáček LJ (2017) FAD regulates cryptochrome protein stability and circadian clock in mice. Cell Rep 19:255–266. https://doi.org/10.1016/j.celrep.2017.03.041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kutta RJ, Archipowa N, Johannissen LO, Jones AR, Scrutton NS (2017) Vertebrate cryptochromes are vestigial flavoproteins. Sci Rep 7:44906. https://doi.org/10.1038/srep44906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schmalen I, Reischl S, Wallach T, Klemz R, Grudziecki A, Prabu JR, Benda C, Kramer A, Wolf E (2014) Interaction of circadian clock proteins CRY1 and PER2 is modulated by zinc binding and disulfide bond formation. Cell 157:1203–1215. https://doi.org/10.1016/j.cell.2014.03.057

    Article  CAS  PubMed  Google Scholar 

  44. Xing W, Busino L, Hinds TR, Marionni ST, Saifee NH, Bush MF, Pagano M, Zheng N (2013) SCF(FBXL3) ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature 496:64–68. https://doi.org/10.1038/nature11964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hirano A, Shi G, Jones CR, Lipzen A, Pennacchio LA, Xu Y, Hallows WC, McMahon T, Yamazaki M, Ptáček LJ, Fu YH (2016) A cryptochrome 2 mutation yields advanced sleep phase in humans. Elife 5:e16695. https://doi.org/10.7554/eLife.16695

    Article  PubMed  PubMed Central  Google Scholar 

  46. Hoang N, Schleicher E, Kacprzak S, Bouly JP, Picot M, Wu W, Berndt A, Wolf E, Bittl R, Ahmad M (2008) Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol 6:e160. https://doi.org/10.1371/journal.pbio.0060160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Foley LE, Gegear RJ, Reppert SM (2011) Human cryptochrome exhibits light-dependent magnetosensitivity. Nat Commun 2:356. https://doi.org/10.1038/ncomms1364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fedele G, Edwards MD, Bhutani S, Hares JM, Murbach M, Green EW, Dissel S, Hastings MH, Rosato E, Kyriacou CP (2014) Genetic analysis of circadian responses to low frequency electromagnetic fields in Drosophila melanogaster. PLoS Genet 10:e1004804. https://doi.org/10.1371/journal.pgen.1004804

    Article  PubMed  PubMed Central  Google Scholar 

  49. Reifler AN, Chervenak AP, Dolikian ME, Benenati BA, Meyers BS, Demertzis ZD, Lynch AM, Li BY, Wachter RD, Abufarha FS, Dulka EA, Pack W, Zhao X, Wong KY (2015) The rat retina has five types of ganglion-cell photoreceptors. Exp Eye Res 130:17–28. https://doi.org/10.1016/j.exer.2014.11.010

    Article  CAS  PubMed  Google Scholar 

  50. Zhao X, Stafford BK, Godin AL, King WM, Wong KY (2014) Photoresponse diversity among the five types of intrinsically photosensitive retinal ganglion cells. J Physiol 592:1619–1636. https://doi.org/10.1113/jphysiol.2013.262782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mure LS, Hatori M, Zhu Q, Demas J, Kim IM, Nayak SK, Panda S (2016) Melanopsin-encoded response properties of intrinsically photosensitive retinal ganglion cells. Neuron 90:1016–1027. https://doi.org/10.1016/j.neuron.2016.04.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lucas RJ, Lall GS, Allen AE, Brown TM (2012) How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock. Prog Brain Res 199:1–18. https://doi.org/10.1016/B978-0-444-59427-3.00001-0

    Article  CAS  PubMed  Google Scholar 

  53. Pérez-Fernández V, Milosavljevic N, Allen AE, Vessey KA, Jobling AI, Fletcher EL, Breen PP, Morley JW, Cameron MA (2019) Rod photoreceptor activation alone defines the release of dopamine in the retina. Curr Biol 29(763–774):e5. https://doi.org/10.1016/j.cub.2019.01.042

    Article  CAS  Google Scholar 

  54. Collins B, Mazzoni EO, Stanewsky R, Blau J (2006) Drosophila cryptochrome is a circadian transcriptional repressor. Curr Biol 16:441–449. https://doi.org/10.1016/j.cub.2006.01.034

    Article  CAS  PubMed  Google Scholar 

  55. Rosensweig C, Reynolds KA, Gao P, Laothamatas I, Shan Y, Ranganathan R, Takahashi JS, Green CB (2018) An evolutionary hotspot defines functional differences between cryptochromes. Nat Commun 9:1138. https://doi.org/10.1038/s41467-018-03503-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kaladchibachi S, Negelspach DC, Fernandez F (2018) Circadian phase-shifting by light: beyond photons. Neurobiol Sleep Circadian Rhythms 5:8–14. https://doi.org/10.1016/j.nbscr.2018.03.003

    Article  PubMed  PubMed Central  Google Scholar 

  57. Vinayak P, Coupar J, Hughes SE, Fozdar P, Kilby J, Garren E, Yoshii T, Hirsh J (2013) Exquisite light sensitivity of Drosophila melanogaster cryptochrome. PLoS Genet 9:e1003615. https://doi.org/10.1371/journal.pgen.100361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Michael AK, Fribourgh JL, Van Gelder RN, Partch CL (2017) Animal cryptochromes: divergent roles in light perception, circadian timekeeping and beyond. Photochem Photobiol 93:128–140. https://doi.org/10.1111/php.12677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Selby CP, Thompson C, Schmitz TM, Van Gelder RN, Sancar A (2000) Functional redundancy of cryptochromes and classical photoreceptors for nonvisual ocular photoreception in mice. Proc Natl Acad Sci USA 97:14697–14702. https://doi.org/10.1073/pnas.260498597

    Article  CAS  PubMed  Google Scholar 

  60. Thompson CL, Blaner WS, Van Gelder RN, Lai K, Quadro L, Colantuoni V, Gottesman ME, Sancar A (2001) Preservation of light signaling to the suprachiasmatic nucleus in vitamin A-deficient mice. Proc Natl Acad Sci USA 98:11708–11713. https://doi.org/10.1073/pnas.201301498

    Article  CAS  PubMed  Google Scholar 

  61. Thompson CL, Selby CP, Van Gelder RN, Blaner WS, Lee J, Quadro L, Lai K, Gottesman ME, Sancar A (2004) Effect of vitamin A depletion on nonvisual phototransduction pathways in cryptochromeless mice. J Biol Rhythms 19:504–517. https://doi.org/10.1177/0748730404270519

    Article  CAS  PubMed  Google Scholar 

  62. Vanderstraeten J, Gailly P, Malkemper EP (2018) Low-light dependence of the magnetic field effect on cryptochromes: possible relevance to plant ecology. Front Plant Sci 9:121. https://doi.org/10.3389/fpls.2018.00121

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are indebted to Martha Daniel for proof reading the manuscript and thankful to three anonymous referees for helpful comments that improved the quality of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Medicine, School of Public Health, Environmental and Work Health Research Center, Université Libre de Bruxelles, CP593, Route de Lennik, 808, 1070, Brussels, Belgium

    Jacques Vanderstraeten

  2. Avenue Constant Montald, 11, 1200, Brussels, Belgium

    Jacques Vanderstraeten

  3. Faculty of Medicine, Institute of Neuroscience (IONS), Cellular and Molecular Pole (CEMO), Catholic University of Louvain, Avenue Mounier 53/B1.53.17, 1200, Brussels, Belgium

    Philippe Gailly

  4. Center of Advanced European Studies and Research (CAESAR), Ludwig-Erhard-Allee 2, Bonn, 53175, Germany

    E. Pascal Malkemper

Authors
  1. Jacques Vanderstraeten
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Gailly
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Pascal Malkemper
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JV developed the hypothesis. All authors wrote the manuscript.

Corresponding author

Correspondence to Jacques Vanderstraeten.

Ethics declarations

Conflict of interest

The authors declare there is no conflict of interest regarding the publication of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vanderstraeten, J., Gailly, P. & Malkemper, E.P. Light entrainment of retinal biorhythms: cryptochrome 2 as candidate photoreceptor in mammals. Cell. Mol. Life Sci. 77, 875–884 (2020). https://doi.org/10.1007/s00018-020-03463-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-020-03463-5

Keywords

Search

Navigation