Photic induction of mPer1 and mPer2 in cry-deficient mice lacking a biological clock

Science

Volumn 286, Issue 5449, 1999, Pages 2531-2534

  Okamura, Hitoshi ^a   Miyake, Shigeru ^a   Sumi, Yasuo ^a   Yamaguchi, Shun ^a   Yasui, Akira ^b   Muijtjens, Manja ^c   Hoeijmakers, Jan H J ^c   Van Der Horst, Gijsbertus T J ^c  

^a KOBE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL RHYTHM; GENE DELETION; GENE EXPRESSION; LIGHT DARK CYCLE; MOUSE; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL CLOCKS; CELL CYCLE PROTEINS; CIRCADIAN RHYTHM; DROSOPHILA PROTEINS; EYE PROTEINS; FEEDBACK; FLAVOPROTEINS; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; LIGHT; LIVER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUTATION; NUCLEAR PROTEINS; PHOTORECEPTORS, INVERTEBRATE; POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RETINA; RNA, MESSENGER; SUPRACHIASMATIC NUCLEUS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 0033601239     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.286.5449.2531     Document Type: Article

References (42)

1. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
2. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
3. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
4. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
5. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
6. J. Dunlap, Cell 96, 271 (1999); S. M. Reppert, Neuron 21, 1 (1998); M. Rosbash et al., Cold Spring Harbor Symp. Quant. Biol. 61, 265 (1996); D. Whitmore, P. Sassone-Corsi, N. S. Foulkes, Curr. Opin. Neurobiol. 8, 635 (1998); L. D. Wilsbacher and J. S. Takahashi, Curr. Opin. Genet. Dev. 8, 595 (1998); M. W. Young, Annu. Rev. Biochem. 67, 135 (1998).
7. H. Tei et al., Nature 389, 512 (1997); Z. S. Sun et al., Cell 90, 1003 (1997).
8. H. Tei et al., Nature 389, 512 (1997); Z. S. Sun et al., Cell 90, 1003 (1997).
9. U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, Cell 91, 1055 (1997); L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997); T. Takumi et al., Genes Cells 3, 167 (1998); T. Takumi et al., EMBO J. 17, 4753 (1998).
10. U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, Cell 91, 1055 (1997); L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997); T. Takumi et al., Genes Cells 3, 167 (1998); T. Takumi et al., EMBO J. 17, 4753 (1998).
11. U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, Cell 91, 1055 (1997); L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997); T. Takumi et al., Genes Cells 3, 167 (1998); T. Takumi et al., EMBO J. 17, 4753 (1998).
12. U. Albrecht, Z. S. Sun, G. Eichele, C. C. Lee, Cell 91, 1055 (1997); L. P. Shearman, M. J. Zylka, D. R. Weaver, L. F. Kolakowski Jr., S. M. Reppert, Neuron 19, 1261 (1997); T. Takumi et al., Genes Cells 3, 167 (1998); T. Takumi et al., EMBO J. 17, 4753 (1998).
13. M. J. Zylka, L. P. Shearman, D. R. Weaver, S. M. Reppert, Neuron 20, 1103 (1998).
14. N. Gekakis et al., Science 280, 1564 (1998); A. M. Sangoram et al., Neuron 21, 1101 (1998).
15. N. Gekakis et al., Science 280, 1564 (1998); A. M. Sangoram et al., Neuron 21, 1101 (1998).
16. R. G. Foster, Neuron 20, 829 (1998).
17. T. Todo et al., Science 272, 109 (1996); P. J. van der Spek et al., Genomics 37, 177 (1996); D. S. Hsu et al., Biochemistry 35, 13871 (1996).
18. T. Todo et al., Science 272, 109 (1996); P. J. van der Spek et al., Genomics 37, 177 (1996); D. S. Hsu et al., Biochemistry 35, 13871 (1996).
19. T. Todo et al., Science 272, 109 (1996); P. J. van der Spek et al., Genomics 37, 177 (1996); D. S. Hsu et al., Biochemistry 35, 13871 (1996).
20. Y. Miyamoto and A. Sancar, Proc. Natl. Acad. Sci. U.S.A. 95, 6097 (1998).
21. G. T. J. van der Horst et al., Nature 398, 630 (1999).
22. R. J. Thresher et al., Science 282, 1490 (1999).
23. K. Kume et al., Cell 98, 193 (1999).
24. -l- animals are arrhythmic, in some of the experiments, we used an absolute time scale rather than a Circadian (CT) or Zeitgeber (ZT) time scale. Circadian expression of mCry1 and mCry2 was studied in Balb-c mice (Japan Animal Care, 8 to 10 weeks old).
25. 14C]-autoradiographic microscale (Amersham). Data from the SCN were normalized with respect to the signal intensities in an equal area of the corpus callosum. The intensities of the optical density of the sections from the rostral-most to the caudal-most of the SCN (10 sections per brain) were then summed; the sum was considered a measure for the amount of mRNA in this region. Values are expressed as means ± SEM (n as indicated in the text). "Relative mRNA abundance" values are calculated assuming a wild-type peak value as 100%.
26. Using the highly sensitive and quantitative "free-floating" method (13), we found a significant difference among six time points in both LD 12:12 [F(5,48) = 5.20, P = 0.023] and DD [F(5,48) = 5.20, P < 0.001] conditions (method: one-way ANOVA).
27. Y. Shigeyoshi et al., Cell 91, 1043 (1997).
28. A. Balsalobre, F. Damiola, U. Schibler, Cell 93, 929 (1998).
29. Quantitative in situ hybridizations on eye sections were performed with the thaw-mounted method. Signals were measured in the external granular layer of the retina (five sections per animal; three independent experiments). Values are expressed as the mean ± SEM.
30. Quantitative PCR was performed with real-time TaqMan technology (PE Biosystems) [C. A. Heid et al., Genome Res. 6, 986 (1996)] and analyzed on an ABI PRISM 7700 (Perkin-Elmer) as described [ T. Takumi et al., Genes Cells 4, 67 (1999)]. Total RNA was extracted from mouse liver with Trizol (Gibco-BRL) and digested with DNAse RQI (Promega). The primers for mPer1 are as follows: Forward 5′-CGCCTCCTTGCTACAGGTAC-3′; Reverse, 5′-GGTAGGAACAGCCAGAGGTTTC-3′, and the TaqMan probe, 5′-CAAAGCCAAAGTCCTTCCCTGCCA-3′. As an internal control for the RNA, expression of GAPDH (glyceraldehyde phosphate dehydrogenase) was examined under the same conditions. Ratios of mPer1 to GAPDH were calculated and normalized. Each value is the mean ± SEM (n = 3).
31. Quantitative PCR was performed with real-time TaqMan technology (PE Biosystems) [C. A. Heid et al., Genome Res. 6, 986 (1996)] and analyzed on an ABI PRISM 7700 (Perkin-Elmer) as described [ T. Takumi et al., Genes Cells 4, 67 (1999)]. Total RNA was extracted from mouse liver with Trizol (Gibco-BRL) and digested with DNAse RQI (Promega). The primers for mPer1 are as follows: Forward 5′-CGCCTCCTTGCTACAGGTAC-3′; Reverse, 5′-GGTAGGAACAGCCAGAGGTTTC-3′, and the TaqMan probe, 5′-CAAAGCCAAAGTCCTTCCCTGCCA-3′. As an internal control for the RNA, expression of GAPDH (glyceraldehyde phosphate dehydrogenase) was examined under the same conditions. Ratios of mPer1 to GAPDH were calculated and normalized. Each value is the mean ± SEM (n = 3).
32. H. Okamura and S. Miyake, data not shown.
33. E. A. Griffin Jr., D. Staknis, C. J. Weitz, Science 286, 768 (1999).
34. mCRY proteins suppress CLOCK/BMAL-mediated transcription from an mPer1 promoter-luciferase reporter construct in HepG2 cells (S. Yamaguchi and H. Okamura, unpublished data).
35. T. Roenneberg and R. G. Foster, Photochem. Photobiol. 66, 549 (1997).
36. M. S. Freedman et al., Science 284, 502 (1999); R. J. Lucas, M. S. Freedman, M. Muñoz, J.-M. Garcia-Fernández, R. G. Foster, Science 284, 505 (1999).
37. M. S. Freedman et al., Science 284, 502 (1999); R. J. Lucas, M. S. Freedman, M. Muñoz, J.-M. Garcia-Fernández, R. G. Foster, Science 284, 505 (1999).
38. Fifty-two hours after initiation of DD exposure (this corresponds to CT16 for wild-type animals), wild-type and mCry1/mCry2 double-mutant mice were exposed to a brief fluorescent light stimulus (600 lux for 30 min). Animals were killed 60, 90, and 120 min, and 4 and 12 hours after the initiation of the light exposure.
39. B. G. Soni and R. G. Foster, FEBS Lett. 406, 279 (1997).
40. I. Provencio, G. Jang, W. J. de Grip, W. P. Hayes, M. D. Rollag, Proc. Natl. Acad. Sci. U.S.A. 95, 340 (1998).
41. M. H. Vitaterna et al., Proc Natl. Acad. Sci. U.S.A. 96, 12114 (1999).
42. We thank T. Takumi, K. Ohata, S. Takekida, H. Onishi, and K. Yagita for support. Supported in part by grants from the Special Coordination Funds of the Science and Technology Agency of Japan; Human Frontier Science; the Louis Jeantet Foundation; the Grant-in-Aid for the Scientific Research on Priority Areas of the Ministry of Education, Science, Sports and Culture of Japan; the Ministry of Welfare of Japan; SRF; and by a Spinoza premium of the Netherlands Organization for Scientific Research (NWO).