Clock-dependent and independent transcriptional control of the two isoforms from the mouse Rorγ gene

Genes to Cells

Volumn 13, Issue 12, 2008, Pages 1197-1210

  Mongrain, Valérie ^a,b   Ruan, Xuan ^a,b   Dardente, Hugues ^a,b,c   Fortier, Erin E ^a,b   Cermakian, Nicolas ^a,b  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RECEPTOR PROTEIN; RETINOIC ACID RELATED ORPHAN RECEPTOR GAMMA PROTEIN; RETINOIC ACID RELATED ORPHAN RECEPTOR GAMMA T PROTEIN; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENZYME ASSAY; GENE EXPRESSION; GENE MUTATION; GENE STRUCTURE; LIVER; MOLECULAR MECHANICS; MOUSE; MUSCLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TESTIS; THYMUS; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL CLOCKS; CERCOPITHECUS AETHIOPS; CLOCK PROTEINS; COS CELLS; GENE EXPRESSION REGULATION; HUMANS; MICE; MUTATION; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; RECEPTORS, RETINOIC ACID; RECEPTORS, THYROID HORMONE; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

MUS;

EID: 57249114501     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2008.01237.x     Document Type: Article

References (52)

1. Abe, M., Herzog, E.D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M. & Block, G.D. (2002) Circadian rhythms in isolated brain regions. J. Neurosci. 22, 350-356.
2. Akashi, M. & Takumi, T. (2005) The orphan nuclear receptor RORα regulated circadian transcription of the mammalian core-clock Bmal1. Nat. Struct. Mol. Biol. 12, 441-448.
3. Alvarez, J.D. & Sehgal, A. (2005) The thymus is similar to the testis in its pattern of circadian clock gene expression. J. Biol. Rhythms 20, 111-121.
4. Alvarez, J.D., Hansen, A., Ord, T., Bebas, P., Chappell, P.E., Giebultowicz, J.M., Williams, C., Moss, S. & Sehgal, A. (2008) The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J. Biol. Rhythms 23, 26-36.
5. Dardente, H. & Cermakian, N. (2007) Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol. Int. 24, 195-213.
6. Dardente, H., Fortier, E.E., Martineau, V. & Cermakian, N. (2007) Cryptochromes impair phosphorylation of transcriptional activators in the clock: A general mechanism for circadian repression. Biochem. J. 402, 525-536.
7. Delaunay, F. & Laudet, V. (2002) Circadian clock and microarrays: mammalian genome gets rhythm. Trends Genet. 18, 595-597.
8. Duffield, G.E. (2003) DNA microarray analyses of circadian timing: The genomic basis of biological time. J. Neuroendocrinol. 15, 991-1002.
9. Eberl, G. & Littman, D.R. (2003) The role of the nuclear hormone receptor ROR γt in the development of lymph nodes and Peyer's patches. Immunol. Rev. 195, 81-90.
10. Eberl, G., Marmon, S., Sunshine, M., Rennert, P.D., Choi, Y. & Littman, D.R. (2004) An essential function for the nuclear receptor RORγ(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5, 64-73.
11. Feillet, C.A., Mendoza, J., Albrecht, U., Pévet, P. & Challet, E. (2008) Forebrain oscillators ticking with different clock hands. Mol. Cell Neurosci. 37, 209-221.
12. Gavanescu, I, Kessler, B, Ploegh, H, Benoist, C. & Mathis, D. (2007) Loss of Aire-dependent thymic expression of a peripheral tissue antigen renders it a target of autoimmunity. Proc. Natl Acad. Sci. USA 104, 4583-4587.
13. Gray, D.H., Chidgey, A.P. & Boyd, R.L. (2002) Analysis of thymic stromal cell populations using flow cytometry. J. Immunol. Methods 260, 15-28.
14. Gréchez-Cassiau, A., Panda, S., Lacoche, S., Teboul, M., Azmi, S., Laudet, V., Hogenesch, J.B., Taneja, R. & Delaunay, F. (2004) The transcriptional repressor STRA13 regulates a subset of peripheral circadian outputs. J. Biol. Chem. 279, 1141-1150.
15. Gréchez-Cassiau, A., Rayet, B., Guillaumond, F., Teboul, M. & Delaunay, F. (2008) The circadian clock component BMAL1 is a critical regulator of p21WAF1/CIP1 expression and hepatocyte proliferation. J. Biol. Chem. 283, 4535-4542.
16. Greiner, E.F., Kirfel, J., Greschik, H., Dorflinger, U., Becker, P., Mercep, A. & Schule, R. (1996) Functional analysis of retinoid Z receptor β, a brain-specific nuclear orphan receptor. Proc. Natl Acad. Sci. USA 93, 10105-10110.
17. Guillaumond, F., Dardente, H., Giguere, V. & Cermakian N. (2005) Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J. Biol. Rhythms 20, 391-403.
18. Hamaguchi, H., Fujimoto, K., Kawamoto, T., Noshiro, M., Maemura, K., Takeda, N., Nagai, R., Furukawa, M., Honma, S., Honma, K., Kurihara, H. & Kato, Y. (2004) Expression of the gene for Dec2, a basic helix-loop-helix transcription factor, is regulated by a molecular clock system. Biochem. J. 382, 43-50.
19. He, Y.M., Deftos, M.L., Ojala, E.W. & Bevan M.J. (1998) ROR γt, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in T cells. Immunity 9, 797-806.
20. Hirose, T., Smith, R.J. & Jetten, A.M. (1994) ROR γ: The third member of ROR/RZR orphan receptor subfamily that is highly expressed in skeletal muscle. Biochem. Biophys. Res. Commun. 205, 1976-1983.
21. Hu, J., Olson, E.N. & Kingston, R.E. (1992) HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Mol. Cell. Biol. 12, 1031-1042.
22. Kang, H.S., Angers, M., Beak, J.Y., Wu, X., Gimble, J.M., Wada, T., Xie, W., Collins, J.B., Grissom, S.F. & Jetten A.M. (2007) Gene expression profiling reveals a regulatory role for RORα and ROR γ in phase I and phase II metabolism. Physiol. Genomics 31, 281-294.
23. Kume, K., Zylka, M.J., Sriram, S., Shearman, L.P., Weaver, D.R., Jin, X., Maywood, E.S., Hastings, M.H. & Reppert, S.M. (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193-205.
24. Kurebayashi, S., Ueda, E., Sakaue, M., Patel, D.D., Medvedev, A., Zhang, F. & Jetten, A.M. (2000) Retinoid-related orphan receptor gamma (ROR γ) is essential for lymphoid organogenesis and controls apoptosis during thymopoiesis. Proc. Natl Acad. Sci. USA 97, 10132-10137.
25. Liu, A.C., Tran, H.G., Zhang, E.E., Priest, A.A., Welsh, D.K. & Kay, S.A. (2008) Redundant function of REV-ERBα and β and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet. 4, e1000023.
26. Liu, A.C., Welsh, D.K., Ko, C.H., Tran, H.G., Zhang, E.E., Priest, A.A., Buhr, E.D., Singer, O., Meeker, K., Verma, I.M., Doyle, F.J. 3rd, Takahashi, J.S. & Kay, S.A. (2007) Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129, 605-616.
27. Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
28. Medvedev, A., Yan, Z.H., Hirose, T., Giguère, V. & Jetten, A.M. (1996) Cloning of a cDNA encoding the murine orphan receptor RZR/ ROR γ and characterization of its response element. Gene 181, 199-206.
29. Morse, D., Cermakian N., Brancorsini, S., Parvinen, M. & Sassone-corsi, P. (2003) No circadian rhythms in testis: Period1 expression is Clock independent and developmentally regulated in the mouse. Mol. Endocrinol. 17, 141-151.
30. Nakahata, Y., Yoshida, M., Takano, A., Soma, H., Yamamoto, T., Yasuda, A., Nakatsu, T. & Takumi, T. (2008) A direct repeat of E-box-like elements is required for cell-autonomous circadian rhythm of clock genes. BMC Mol. Biol. 9, 1.
31. Noshiro, M., Furukawa, M., Honma, S., Kawamoto, T., Hamada, T., Honma, K. & Kato, Y. (2005) Tissue-specific disruption of rhythmic expression of Dec1 and Dec2 in Clock mutant mice. J Biol. Rhythms 20, 404-418.
32. Oishi, K., Fukui, H. & Ishida, N. (2000) Rhythmic expression of Bmal1 mRNA is altered in Clock mutant mice: Differential regulation in the suprachiasmatic nucleus and peripheral tissues. Biochem. Biophys. Res. Commun. 268, 164-171.
33. Panda, S., Antoch, M.P., Miller, B.H., Su, A.I., Schook, A.B., Straume, M., Schultz, P.G., Kay, S.A., Takahashi, J.S. & Hogenesch, J.B. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307-320.
34. Preitner, N., Daminola, F.L., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U. & Schibler, U. (2002) The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260.
35. Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., Mcnamara, P., Naik, K.A., FitzGerald, G.A., Kay, S.A. & Hogenesch, J.B. (2004) A functional genomics strategy reveals Rorα as a component of the mammalian circadian clock. Neuron 43, 527-537.
36. Sato, T.K., Yamada, R.G., Ukai, H., Baggs, J.E., Miraglia, L.J., Kobayashi, T.J., Welsh, D.K., Kay, S.A., Ueda, H.R. & Hogenesch, J.B. (2006) Feedback repression is required for mammalian circadian clock function. Nat. Genet. 38, 312-319.
37. Schibler, U., Ripperger, J. & Brown, S.A. (2003) Peripheral circadian oscillators in mammals: Time and food. J. Biol. Rhythms 18, 250-260.
38. Storch, K.F., Lipan, O., Leykin, I., Viswanathan, N., Davis, F.C., Wong, W.H. & Weitz, C.J. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78-83.
39. Sumi, Y., Yagita, K., Yamaguchi, S., Ishida, Y., Kuroda, Y. & Okamura, H. (2002) Rhythmic expression of RORβ mRNA in the mice suprachiasmatic nucleus. Neurosci. Lett. 320, 13-16.
40. Sun, A., Unutmaz, D., Zou, Y., Sunshine, M.J., Pierani, A., Brenner-Morton, S., Mebius, R.E. & Littman, D.R. (2000) Requirement for ROR γ in thymocyte survival and lymphoid organ development. Science 288, 2369-2373.
41. Travnickova-Bendova, Z., Cermakian, N., Reppert S.M. & Sassone-Corsi, P. (2002). Bimodal regulation of mPeriod promoters by CREB-dependent signalling and CLOCK: BMAL1 activity. Proc. Natl Acad. Sci. USA 99, 7728-7733.
42. Ueda, H.R., Chen, W., Adachi, A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Nakahama, K.-I., Suzuki, Y., Sugano, S., Iino, M., Shigeyoshi, Y. & Hashimoto, S. (2002) A transcription factor response element for gene expression during circadian night. Nature 418, 534-539.
43. Ueda, H.R., Hayashi, S., Chen, W., Sano, M., Machida, M., Shigeyoshi, Y., Iino, M. & Hashimoto, S. (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat. Genet. 37, 167-192.
44. Villey, I., Chasseval, R. & Villartay, J. (1999) ROR γT, a thymus-specific isoform of the orphan nuclear receptor ROR γ/TOR, is up-regulated by signaling through the pre-T cell receptor and binds to the TEA promoter. Eur. J. Immunol. 29, 4072-4080.
45. Vitaterna, M.H., King, D.P., Chang, A., Kornhauser, J.M., Lowrey, P.L., McDonald, J.D., Dove, W.F., Pinto, L.H., Turek, F.W. & Takahadhi, J.S. (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behaviour. Science 264, 719-725.
46. Welsh, D.K., Yoo, S.H., Liu, A.C., Takahashi, J.S. & Kay, S.A. (2004) Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr. Biol. 14, 2289-2295.
47. Xi, H., Schwartz, R., Engel, I., Murre, C. & Kersh, G.J. (2006) Interplay between ROR γt, Egr3, and E-proteins controls proliferation in response to pre-TCR signals. Immunity 24, 813-826.
48. Yamamoto, T., Nakahata, Y., Soma, H., Akashi, M., Mamine, T. & Takumi, T. (2004) Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Mol. Biol. 5, 18-26.
49. Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G.D., Sakaki, Y., Menaker, M. & Tei, H. (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685.
50. Yang, X., Downes, M., Yu, R.T., Bookout, A.L., He, W., Straume, M., Mangelsdorf, D.J. & Evans, R.M. (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell 126, 801-810.
51. Yoo, S.H., Ko, C.H., Lowrey, P.L., Buhr, E.D., Song, E.J., Chang, S., Yoo, O.J., Yamazaki, S., Lee, C. & Takahashi, J.S. (2005) A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo. Proc. Natl Acad. Sci. USA 102, 2608-2613.
52. Yoo, S.H., Yamazaki, S., Lowrey, P.L., Shimomura, K., Ko, C.H., Buhr, E.D., Siepka, S.M., Hong, H.K., Oh, W.J., Yoo, O.J., Menaker, M. & Takahashi, J.S. (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl Acad. Sci. USA 101, 5339-5346.