Cryptochromes: Sensory reception, transduction, and clock functions subserving circadian systems

Current Opinion in Neurobiology

Volumn 10, Issue 4, 2000, Pages 456-466

  Hall, Jeffrey C ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; RHODOPSIN; UNCLASSIFIED DRUG; VISUAL PROTEINS AND PIGMENTS;

BEHAVIORAL SCIENCE; BRAIN; CIRCADIAN RHYTHM; CODON; DROSOPHILA; GENE MUTATION; GENETIC TRANSDUCTION; LIGHT ABSORPTION; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; REVIEW; SENSORY RECEPTOR; SUPRACHIASMATIC NUCLEUS; VERTEBRATE;

EID: 0033867715     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00117-3     Document Type: Review

References (56)

1. Cashmore A.R., Jarillo J.A., Wu Y-J., Liu D. Cryptochromes: blue light receptors for plants and animals. Science. 284:1999;760-765. This review includes discussions of the first known cryptochrome mutants. Such plant variants were not called 'cry' mutants originally, because they were first identified by way of their blue-light-induced hypocotyl elongation (hy4) phenotype. Subsequently, hy4 mutations were shown to define the cry1 gene of plants, and the fha late-flowering variants were shown to be mutated in cry2. The other colors to which plant tissues respond are red and far-red light, reception of which is mediated by phytochromes; however, these substances are also blue-light photoreceptors, as is the flavin-containing nonphototropic hypocotyl (NHP1) photoreceptive protein (also known as phototropin).
2. Sancar A. Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu Rev Biochem. 69:2000;31-67.
3. Van Gelder R.N. Circadian rhythms: eyes of the clock. Curr Biol. 8:1998;R798-R801.
4. Lucas R.J., Foster R.G. Circadian clocks: a cry in the dark? Curr Biol. 9:1999;R825-R828.
5. Lucas R.J., Foster R.G. Photoentrainment in mammals: a role for cryptochrome? J Biol Rhythms. 14:1999;4-10.
6. Whitmore D., Sassone-Corsi P. Cryptic clues to clock function. Nature. 398:1999;557-558.
7. Hardin P.E., Glossop N.R.J. The CRYs of flies and mice. Science. 286:1999;2460-2461.
8. Emery P., So W.V., Kaneko M., Hall J.C., Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell. 95:1998;669-679.
9. b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell. 95:1998;681-692.
10. Giebultowicz J.M., Stanewsky R., Hall J.C., Hege D.M. Transplanted Drosophila excretory tubules maintain circadian clock cycling out of phase with the host. Curr Biol. 10:2000;107-110. One feature of this study reinforced the fact that oscillations of clock-gene expression are most conveniently monitored in tissues carrying portions of clock genes fused to luciferase (luc)-encoding sequences. Autonomous per-luc cycling in body parts was first documented in [13] and was further demonstrated by Giebultowicz et al. for cultured internal tissues carrying a tim-luc fusion transgene (also shown for an appendage in [14]).
11. b-induced circadian blindness, is problematical. The histological results just noted jibe with the most recent examination in tissue extracts of free-running rhythmicity for TIM oscillations, in which robust protein cycling was not long-lived in constant darkness [53].
12. Krishnan B., Dryer S.E., Hardin P.E. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature. 400:1999;375-378.
13. Plautz J.D., Kaneko M., Hall J.C., Kay S.A. Independent photoreceptive circadian clocks throughout Drosophila. Science. 278:1997;1632-1635.
14. th Meeting of the Society for Research on Biological Rhythms: 2000 May 10-13, Jacksonville FL. Jacksonville FL: Society for Research on Biological Rhythms; 150:97.
15. Okano S., Kanno S-i., Takao M., Eker A.P.M., Isono K., Tsukahara Y., Yasui A. A putative blue-light receptor from Drosophila melanogaster. Photochem Photobiol. 69:1999;108-113.
16. Ishikawa T., Matsumoto A., Kato T. Jr., Togashi S., Ryo H., Ikenaga M., Todo T., Ueda R., Tanimura T. DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Genes Cells. 4:1999;57-65.
17. + more broadly (by driving it with a tim-gal4 transgene) led to at least partial restoration of TIM cycling in whole-head or fly-body extracts.
18. Park J.H., Helfrich-Förster C., Lee G., Liu L., Rosbash M., Hall J.C. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA. 97:2000;3608-3613.
19. •].
20. Emery P., Stanewsky R., Hall J.C., Rosbash M. A unique circadian-rhythm photoreceptor. Nature. 404:2000;456-457.
21. Ceriani M.F., Darlington T.K., Staknis D., Mas P., Petti A.A., Weitz C.J., Kay S.A. Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science. 285:1999;553-556.
22. Naidoo N., Song W., Hunter-Ensor M., Sehgal A. A role for the proteasome in the light response of the timeless clock protein. Science. 285:1999;1737-1741.
23. Helfrich-Förster C. Photic entrainment in Drosophila's activity rhythm occurs by retinal and extraretinal pathways. Biol Rhythm Res. 28(suppl):1997;119.
24. Ohata K., Nishiyama H., Tsukahara Y. Action spectrum of the circadian clock photoreceptor in Drosophila melanogaster. Touitou Y. Biological Clocks: Mechanisms and Applications. 1998;167-170 Elsevier, Amsterdam.
25. Zimmerman W.F., Goldsmith T.H. Photosensitivity of the circadian rhythm and of visual receptors in carotenoid-depleted Drosophila. Science. 171:1971;1167-1169.
26. Yasuyama K., Meinertzhagen I.A. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J Comp Neurol. 412:1999;193-202. Cells within this eyelet project axons to the vicinity of pacemaker neurons in the adult brain. The H-B cell bodies also contain rhodopsin (one of seven forms known in this organism by identification of opsin-encoding 'Rh' sequences). The principal locations of their expression are within photoreceptor cells of the compound eyes and ocelli, although one of the fly's Rh genes is also active in the male reproductive system [54]. It is important to mention this result, lest we get carried away with the notion that 'body photoreception' is necessarily mediated solely by cryptochrome.
27. Helfrich-Förster, C., Stanewsky, R., Emery, P., Hofbauer, A., Rosbash, M., Hall, J.C.Entrainment of Drosophila's activity rhythm by multiple photoreceptors. At URL: http://helios.bto.ed.ac.uk/icapd/btl/meeting/html .
28. Short mutation on phase shifts induced by light pulses delivered to Drosophila larvae. J Biol Rhythms. 15:2000;13-30.
29. Mrosovsky N. Locomotor activity and non-photic influences on circadian clocks. Biol Rev. 71:1996;343-372.
30. Foster R.G. Shedding light on the biological clock. Neuron. 20:1998;829-832.
31. Campbell S.S., Murphy P.J. Extraocular circadian phototransduction in humans. Science. 279:1998;396-399.
32. Meijer J.H., Thio B., Albus H., Schaap J., Ruijs A.C.J. Functional absence of extraocular photoreception in hamster circadian rhythm entrainment. Brain Res. 831:1999;337-339.
33. Yamazaka S., Goto M., Menaker M. No evidence for extraocular photoreceptors in the circadian system of the Syrian hamster. J Biol Rhythms. 14:1999;197-201.
34. Lindblom N., Heiskala H., Hätönen T., Mustanoja S., Alfthan H., Alila-Johansson A., Laakso M-J. No evidence for extraocular light induced phase shifting of human melatonin, cortisol and thyrotropin rhythms. Neuroreport. 11:2000;713-717.
35. Freedman M.S., Lucas R.J., Soni B., von Schantz M., Muñoz M., David-Gray Z., Foster R. Regulation of mammalian circadian behavior by non-rod, non-cone, ocular photoreceptors. Science. 284:1999;502-504.
36. Provencio I., Rodriguez I.R., Jiang G., Hayes W.P., Moreira E.F., Rollag M.D. A novel human opsin in the inner retina. J Neurosci. 20:2000;600-605. Occult forms of opsins are known in other vertebrates as well (most recently [55]). Here they may be involved in both ocular photoreception, which could feed into the brain's clock, and extra-ocular photoreception. Indeed, 'vertebrate ancient-long opsin' in zebrafish is found both in the eye and the diencephalon [55].
37. Provencio I., Cooper H.M., Foster R.G. Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. J Comp Neurol. 395:1998;417-439.
38. Yoshimura T., Ebihara S. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+) mice. J Comp Physiol A. 178:1996;791-802.
39. Yoshimura T., Ebihara S. Decline of circadian photosensitivity associated with retinal degeneration in CBA/J-rd/rd mice. Brain Res. 779:1998;188-193.
40. Pittler S.J., Keeler C.E., Sidman R.L., Baehr W. PCR analysis of DNA from 70-year-old sections of rodless retina demonstrates identity with the mouse rd defect. Proc Natl Acad Sci USA. 90:1993;9616-9619.
41. 2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proc Natl Acad Sci USA. 95:1998;6097-6102.
42. Field M.D., Maywood E.S., O'Brien J.A., Waever D.R., Reppert S.M., Hastings M.H. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron. 25:2000;437-447.
43. Dunlap J.C. Molecular bases for circadian clocks. Cell. 96:1999;271-290.
44. Whitmore D., Foulkes N.S., Sassone-Corsi P. Light acts directly on organs and cells to set the vertebrate circadian clock. Nature. 404:2000;87-91.
45. van der Horst G.T.J., Muijtjens M., Kobayashi K., Takano R., Kanno S-i., Takao M., de Wit J., Verkerk A., Eker A.P.M., van Leenen D.et al. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature. 398:1999;627-663.
46. Griffin E.A.Jr., Staknis D., Weitz C.J. Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science. 286:1999;768-771.
47. Kume K., Zylka M.J., Sriram S., Shearman L.P., Weaver D.R., Jin Z., Maywood E.S., Hastings M.H., Reppert S.M. mCRY1 and mCRY2 are essential components of the negative limb of the circadian feedback loop. Cell. 98:1999;193-205.
48. Shearman L.P., Sriram S., Weaver D.R., Maywood E.S., Chaves D., Zheng B., Kume K., Lee C.C., van der Horst T.J., Hastings M.H., Reppert S.M. Interacting molecular loops in the mammalian circadian clock. Science. 288:2000;1013-1019.
49. Miyamoto Y., Sancar A. Circadian regulation of cryptochrome genes in the mouse. Mol Brain Res. 71:1999;238-243.
50. Vitaterna M.H., Selby C.P., Todo T., Niwa H., Thompson C., Fruechte E.M., Hitomi K., Thresher R.J., Ishikawa T., Miyazaki J.et al. Differential regulation of mammalian Period genes and circadian rhythmicity by cryptochromes 1 and 2. Proc Natl Acad Sci USA. 96:1999;12114-12119.
51. Thresher R.J., Vitaterna M.H., Miyamoto Y., Kazantsev A., Hsu D.S., Petit C., Selby C.P., Dawut L., Smithies O., Takahashi J.S., Sancar A. Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. Science. 282:1998;1490-1494.
52. Okamura H., Miyake S., Sumi Y., Yamaguchi S., Yasui A., Miujtjens M., Hoeijmakers J.H.J., van der Horst G.T.J. Photic induction of mPer1 and mPer2 in Cry-deficient mice lacking a biological clock. Science. 286:1999;2531-2534.
53. Price J.L., Blau J., Rothenfluh A., Abodeely M., Kloss B., Young M.W. double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell. 94:1998;83-95.
54. Alvarez C.E., Robison K., Gilbert W. Novel Gqα isoform is a candidate transducer of rhodopsin signaling in a Drosophila testes-autonomous pacemaker. Proc Natl Acad Sci USA. 93:1996;12278-12282.
55. Kojima D., Mano H., Fukada Y. Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells. J Neurosci. 20:2000;2845-2851.
56. Benna C., Scannapieco P., Piccin A., Sandrelli F., Zordan M., Rosato E., Kyriacou C.P., Valle G., Costa R. A second timeless gene in Drosophila shares greater sequence similarity with mammalian tim. Curr Biol. 2000;. in press.