Lauren P. Shearman, ^1* Sathyanarayanan Sriram, ^1* David R. Weaver, ¹ Elizabeth S. Maywood, ² Ins Chaves, ³ Binhai Zheng, ⁴ Kazuhiko Kume, ¹ Cheng Chi Lee, ⁴ Gijsbertus T. J. van der , Horst, ³ Michael H. Hastings, ² Steven M. Reppert ¹

We show that, in the mouse, the core mechanism for the master circadian clock consists of interacting positive and negative transcription and translation feedback loops. Analysis of Clock/Clock mutant mice, homozygous Period2^Brdm1 mutants, and Cryptochrome-deficient mice reveals substantially altered Bmal1 rhythms, consistent with a dominant role of PERIOD2 in the positive regulation of the Bmal1 loop. In vitro analysis of CRYPTOCHROME inhibition of CLOCK: BMAL1-mediated transcription shows that the inhibition is through direct protein:protein interactions, independent of the PERIOD and TIMELESS proteins. PERIOD2 is a positive regulator of the Bmal1 loop, and CRYPTOCHROMES are the negative regulators of the Period and Cryptochrome cycles.

¹ Laboratory of Developmental Chronobiology, MassGeneral Hospital for Children, Massachusetts General Hospital, and Harvard Medical School, Boston, MA 02114, USA.
² Department of Anatomy, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK.
³ Medical Genetic Center, Department of Cell Biology and Genetics, Erasmus University, 3000 DR Rotterdam, Netherlands.
⁴ Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
^*   These authors contributed equally to this work.

   To whom correspondence should be addressed. E-mail: reppert{at}helix.mgh.harvard.edu

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Presentation of the 2012 Paleontological Society Medal to Bill Schopf.

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Identification of functional clock-controlled elements involved in differential timing of Per1 and Per2 transcription.

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Exposure of Pregnant Rats to Restricted Feeding Schedule Synchronizes the SCN Clocks of Their Fetuses under Constant Light but Not under a Light-Dark Regime.

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Physiology of Circadian Entrainment.

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M. Stratmann, F. Stadler, F. Tamanini, G. T. J. van der Horst, and J. A. Ripperger (2010)
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Melatonin Sensitizes Human Myometrial Cells to Oxytocin in a Protein Kinase C{alpha}/Extracellular-Signal Regulated Kinase-Dependent Manner.

J. T. Sharkey, C. Cable, and J. Olcese (2010)
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Cryptochromes--a potential magnetoreceptor: what do we know and what do we want to know?.

M. Liedvogel and H. Mouritsen (2010)
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DYRK1A and Glycogen Synthase Kinase 3{beta}, a Dual-Kinase Mechanism Directing Proteasomal Degradation of CRY2 for Circadian Timekeeping.

N. Kurabayashi, T. Hirota, M. Sakai, K. Sanada, and Y. Fukada (2010)
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Different mechanisms of adjustment to a change of the photoperiod in the suprachiasmatic and liver circadian clocks.

S. Sosniyenko, D. Parkanova, H. Illnerova, M. Sladek, and A. Sumova (2010)
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Role of mutation of the circadian clock gene Per2 in cardiovascular circadian rhythms.

A. Vukolic, V. Antic, B. N. Van Vliet, Z. Yang, U. Albrecht, and J.-P. Montani (2010)
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Regulation of circadian gene expression in the kidney by light and food cues in rats.

T. Wu, Y. Ni, Y. Dong, J. Xu, X. Song, H. Kato, and Z. Fu (2010)
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Attenuation of myocardial injury in mice with functional deletion of the circadian rhythm gene mPer2.

J. A. I. Virag, J. L. Dries, P. R. Easton, A. M. Friesland, J. H. DeAntonio, V. Chintalgattu, E. Cozzi, B. D. Lehmann, J. M. Ding, and R. M. Lust (2010)
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The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors.

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Circadian Expression of Clock Genes in Two Mosquito Disease Vectors: cry2 Is Different.

C. Gentile, G. B. S. Rivas, A. C. A. Meireles-Filho, J. B. P. Lima, and A. A. Peixoto (2009)
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Circadian Disruption, Per3, and Human Cytokine Secretion.

J. Guess, J. B. Burch, K. Ogoussan, C. A. Armstead, Hongmei Zhang, S. Wagner, J. R. Hebert, P. Wood, S. D. Youngstedt, L. J. Hofseth, et al. (2009)
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How nuclear receptors tell time.

M. Teboul, A. Grechez-Cassiau, F. Guillaumond, and F. Delaunay (2009)
J Appl Physiol 107, 1965-1971
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ID2 (Inhibitor of DNA Binding 2) Is a Rhythmically Expressed Transcriptional Repressor Required for Circadian Clock Output in Mouse Liver.

T. Y. Hou, S. M. Ward, J. M. Murad, N. P. Watson, M. A. Israel, and G. E. Duffield (2009)
J. Biol. Chem. 284, 31735-31745
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Proximate mechanisms driving circadian control of neuroendocrine function: Lessons from the young and old.

W. P. Williams III, E. M. Gibson, C. Wang, S. Tjho, N. Khattar, G. E. Bentley, K. Tsutsui, and L. J. Kriegsfeld (2009)
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Generation of a Novel Allelic Series of Cryptochrome Mutants via Mutagenesis Reveals Residues Involved in Protein-Protein Interaction and CRY2-Specific Repression.

E. V. McCarthy, J. E. Baggs, J. M. Geskes, J. B. Hogenesch, and C. B. Green (2009)
Mol. Cell. Biol. 29, 5465-5476
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Effects of acute hypoxia and hyperthermia on the permeability of the blood-brain barrier in adult rats.

S. S. Natah, S. Srinivasan, Q. Pittman, Z. Zhao, and J. F. Dunn (2009)
J Appl Physiol 107, 1348-1356
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A Role for the Clock Gene Per1 in Prostate Cancer.

Q. Cao, S. Gery, A. Dashti, D. Yin, Y. Zhou, J. Gu, and H. P. Koeffler (2009)
Cancer Res. 69, 7619-7625
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Rhythmic Expression of MicroRNA-26a Regulates the L-type Voltage-gated Calcium Channel {alpha}1C Subunit in Chicken Cone Photoreceptors.

L. Shi, M. L. Ko, and G. Y.-P. Ko (2009)
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Negative feedback maintenance of heme homeostasis by its receptor, Rev-erb{alpha}.

N. Wu, L. Yin, E. A. Hanniman, S. Joshi, and M. A. Lazar (2009)
Genes & Dev. 23, 2201-2209
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Preferential Inhibition of BMAL2-CLOCK Activity by PER2 Reemphasizes Its Negative Role and a Positive Role of BMAL2 in the Circadian Transcription.

M. Sasaki, H. Yoshitane, N.-H. Du, T. Okano, and Y. Fukada (2009)
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A model of the cell-autonomous mammalian circadian clock.

H. P. Mirsky, A. C. Liu, D. K. Welsh, S. A. Kay, and F. J. Doyle III (2009)
PNAS 106, 11107-11112
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Daily rhythms of food-anticipatory behavioral activity do not require the known circadian clock.

K.-F. Storch and C. J. Weitz (2009)
PNAS 106, 6808-6813
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Clock Gene Mouse Period2 Overexpression Inhibits Growth of Human Pancreatic Cancer Cells and Has Synergistic Effect with Cisplatin.

A. ODA, Y. KATAYOSE, S. YABUUCHI, K. YAMAMOTO, M. MIZUMA, S. SHIRASOU, T. ONOGAWA, H. OHTSUKA, H. YOSHIDA, H. HAYASHI, et al. (2009)
Anticancer Res 29, 1201-1209
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A large-scale functional RNAi screen reveals a role for CK2 in the mammalian circadian clock.

B. Maier, S. Wendt, J. T. Vanselow, T. Wallach, S. Reischl, S. Oehmke, A. Schlosser, and A. Kramer (2009)
Genes & Dev. 23, 708-718
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Molecular characterization of Mybbp1a as a co-repressor on the Period2 promoter.

Y. Hara, Y. Onishi, K. Oishi, K. Miyazaki, A. Fukamizu, and N. Ishida (2009)
Nucleic Acids Res. 37, 1115-1126
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Melatonin Synergizes with Oxytocin to Enhance Contractility of Human Myometrial Smooth Muscle Cells.

J. T. Sharkey, R. Puttaramu, R. A. Word, and J. Olcese (2009)
J. Clin. Endocrinol. Metab. 94, 421-427
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Circadian Rhythm of Osteocalcin in the Maxillomandibular Complex.

Y. Gafni, A. A. Ptitsyn, Y. Zilberman, G. Pelled, J. M. Gimble, and D. Gazit (2009)
Journal of Dental Research 88, 45-50
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Mouse period 2 mRNA circadian oscillation is modulated by PTB-mediated rhythmic mRNA degradation.

K.-C. Woo, T.-D. Kim, K.-H. Lee, D.-Y. Kim, W. Kim, K.-Y. Lee, and K.-T. Kim (2009)
Nucleic Acids Res. 37, 26-37
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Closing the circadian negative feedback loop: FRQ-dependent clearance of WC-1 from the nucleus.

C. I. Hong, P. Ruoff, J. J. Loros, and J. C. Dunlap (2008)
Genes & Dev. 22, 3196-3204
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Maternal Control of the Fetal and Neonatal Rat Suprachiasmatic Nucleus.

R. El-Hennamy, K. Mateju, Z. Bendova, S. Sosniyenko, and A. Sumova (2008)
J Biol Rhythms 23, 435-444
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Diurnal variations in myocardial metabolism.

M. S. Bray and M. E. Young (2008)
Cardiovasc Res 79, 228-237
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Identification of novel genes involved in light-dependent CRY degradation through a genome-wide RNAi screen.

S. Sathyanarayanan, X. Zheng, S. Kumar, C.-H. Chen, D. Chen, B. Hay, and A. Sehgal (2008)
Genes & Dev. 22, 1522-1533
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Rhythmic SAF-A Binding Underlies Circadian Transcription of the Bmal1 Gene.

Y. Onishi, S. Hanai, T. Ohno, Y. Hara, and N. Ishida (2008)
Mol. Cell. Biol. 28, 3477-3488
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Genetic Components of the Circadian Clock Regulate Thrombogenesis In Vivo.

E. J. Westgate, Y. Cheng, D. F. Reilly, T. S. Price, J. A. Walisser, C. A. Bradfield, and G. A. FitzGerald (2008)
Circulation 117, 2087-2095
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Disruption of Clock Gene Expression Alters Responses of the Aryl Hydrocarbon Receptor Signaling Pathway in the Mouse Mammary Gland.

X. Qu, R. P. Metz, W. W. Porter, V. M. Cassone, and D. J. Earnest (2007)
Mol. Pharmacol. 72, 1349-1358
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Knockdown of clock genes in the suprachiasmatic nucleus blocks prolactin surges and alters FRA expression in the locus coeruleus of female rats.

M. O. Poletini, D. T. McKee, J. E. Kennett, J. Doster, and M. E. Freeman (2007)
Am J Physiol Endocrinol Metab 293, E1325-E1334
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Circadian Rhythm Gene Regulation in the Housefly Musca domestica.

V. Codd, D. Dolezel, J. Stehlik, A. Piccin, K. J. Garner, S. N. Racey, K. R. Straatman, E. J. Louis, R. Costa, I. Sauman, et al. (2007)
Genetics 177, 1539-1551
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Circadian control by the reduction/oxidation pathway: Catalase represses light-dependent clock gene expression in the zebrafish.

J. Hirayama, S. Cho, and P. Sassone-Corsi (2007)
PNAS 104, 15747-15752
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{beta}-TrCP1-Mediated Degradation of PERIOD2 Is Essential for Circadian Dynamics.

S. Reischl, K. Vanselow, P. O. Westermark, N. Thierfelder, B. Maier, H. Herzel, and A. Kramer (2007)
J Biol Rhythms 22, 375-386
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Up-regulation of Per1 expression by estradiol and progesterone in the rat uterus.

P.-J. He, M. Hirata, N. Yamauchi, and M.-a. Hattori (2007)
J. Endocrinol. 194, 511-519
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Tumor Suppression and Circadian Function.

M. Chen-Goodspeed and Cheng Chi Lee (2007)
J Biol Rhythms 22, 291-298
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Multifactorial Regulation of Daily Rhythms in Expression of the Metabolically Responsive Gene Spot14 in the Mouse Liver.

A. Ishihara, E. Matsumoto, K. Horikawa, T. Kudo, E. Sakao, A. Nemoto, K. Iwase, H. Sugiyama, Y. Tamura, S. Shibata, et al. (2007)
J Biol Rhythms 22, 324-334
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The disruption of circadian clockwork in differentiating cells from rat reproductive tissues as identified by in vitro real-time monitoring system.

P.-J. He, M. Hirata, N. Yamauchi, S. Hashimoto, and M.-a. Hattori (2007)
J. Endocrinol. 193, 413-420
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Dynamics of the Adjustment of Clock Gene Expression in the Rat Suprachiasmatic Nucleus to an Asymmetrical Change from a Long to a Short Photoperiod.

A. Sumova, Z. Kovacikova, and H. Illnerova (2007)
J Biol Rhythms 22, 259-267
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SCFFbxl3 Controls the Oscillation of the Circadian Clock by Directing the Degradation of Cryptochrome Proteins.

L. Busino, F. Bassermann, A. Maiolica, C. Lee, P. M. Nolan, S. I. H. Godinho, G. F. Draetta, and M. Pagano (2007)
Science 316, 900-904
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TIME FOR COFFEE Encodes a Nuclear Regulator in the Arabidopsis thaliana Circadian Clock.

Z. Ding, A. J. Millar, A. M. Davis, and S. J. Davis (2007)
PLANT CELL 19, 1522-1536
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Phase Sensitivity Analysis of Circadian Rhythm Entrainment.

R. Gunawan and F. J. Doyle III (2007)
J Biol Rhythms 22, 180-194
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Inter-subject differences in constitutive expression levels of the clock gene in man.

A. J Balmforth, P. J Grant, E. M Scott, S. B Wheatcroft, M. T Kearney, B. Staels, and N. Marx (2007)
Diabetes and Vascular Disease Research 4, 39-43
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Circadian variation of blood pressure and the vascular response to asynchronous stress.

A. M. Curtis, Y. Cheng, S. Kapoor, D. Reilly, T. S. Price, and G. A. FitzGerald (2007)
PNAS 104, 3450-3455
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The Multiple Facets of Per2.

U. Albrecht, A. Bordon, I. Schmutz, and J. Ripperger (2007)
Cold Spring Harb Symp Quant Biol 72, 95-104
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Structure Function Analysis of Mammalian Cryptochromes.

F. Tamanini, I. Chaves, M. I. Bajek, and G. T. J. van der Horst (2007)
Cold Spring Harb Symp Quant Biol 72, 133-139
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Posttranslational Control of the Neurospora Circadian Clock.

J. Cha, G. Huang, J. Guo, and Y. Liu (2007)
Cold Spring Harb Symp Quant Biol 72, 185-191
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Complexity of the Neurospora crassa Circadian Clock System: Multiple Loops and Oscillators.

R. M. de Paula, M. W. Vitalini, R. H. Gomer, and D. Bell-Pedersen (2007)
Cold Spring Harb Symp Quant Biol 72, 345-351
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Systems Biology of Mammalian Circadian Clocks.

H. R. Ueda (2007)
Cold Spring Harb Symp Quant Biol 72, 365-380
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Nuclear Receptors, Metabolism, and the Circadian Clock.

X. Yang, K. A. Lamia, and R. M. Evans (2007)
Cold Spring Harb Symp Quant Biol 72, 387-394
 |  Abstract »  |  PDF »

The Role of Circadian Regulation in Cancer.

S. Gery and H. P. Koeffler (2007)
Cold Spring Harb Symp Quant Biol 72, 459-464
 |  Abstract »  |  PDF »

Glucocorticoid Regulation of 24-Hour Oscillation in Interferon Receptor Gene Expression in Mouse Liver.

S. Koyanagi, H. Suyama, Y. Kuramoto, N. Matsunaga, H. Takane, S. Soeda, H. Shimeno, S. Higuchi, and S. Ohdo (2006)
Endocrinology 147, 5034-5040
 |  Abstract »  |  Full Text »  |  PDF »

Molecular components of the mammalian circadian clock.

C. H. Ko and J. S. Takahashi (2006)
Hum. Mol. Genet. 15, R271-R277
 |  Abstract »  |  Full Text »  |  PDF »

BMAL1 Shuttling Controls Transactivation and Degradation of the CLOCK/BMAL1 Heterodimer.

I. Kwon, J. Lee, S. H. Chang, N. C. Jung, B. J. Lee, G. H. Son, K. Kim, and K. H. Lee (2006)
Mol. Cell. Biol. 26, 7318-7330
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Functional central rhythmicity and light entrainment, but not liver and muscle rhythmicity, are Clock independent.

D. J. Kennaway, J. A. Owens, A. Voultsios, and T. J. Varcoe (2006)
Am J Physiol Regulatory Integrative Comp Physiol 291, R1172-R1180
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Circadian Clock Gene Expression in the Ovary: Effects of Luteinizing Hormone.

B. N. Karman and S. A. Tischkau (2006)
Biol Reprod 75, 624-632
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Differential effects of PER2 phosphorylation: molecular basis for the human familial advanced sleep phase syndrome (FASPS).

K. Vanselow, J. T. Vanselow, P. O. Westermark, S. Reischl, B. Maier, T. Korte, A. Herrmann, H. Herzel, A. Schlosser, and A. Kramer (2006)
Genes & Dev. 20, 2660-2672
 |  Abstract »  |  Full Text »  |  PDF »

CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop.

Q. He, J. Cha, Q. He, H.-C. Lee, Y. Yang, and Y. Liu (2006)
Genes & Dev. 20, 2552-2565
 |  Abstract »  |  Full Text »  |  PDF »

Circadian Rhythms in Neurospora crassa and Other Filamentous Fungi.

Y. Liu and D. Bell-Pedersen (2006)
Eukaryot. Cell 5, 1184-1193
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Reciprocal Regulation of Brain and Muscle Arnt-Like Protein 1 and Peroxisome Proliferator-Activated Receptor {alpha} Defines a Novel Positive Feedback Loop in the Rodent Liver Circadian Clock.

L. Canaple, J. Rambaud, O. Dkhissi-Benyahya, B. Rayet, N. S. Tan, L. Michalik, F. Delaunay, W. Wahli, and V. Laudet (2006)
Mol. Endocrinol. 20, 1715-1727
 |  Abstract »  |  Full Text »  |  PDF »

Diurnal Rhythmicity of the Clock Genes Per1 and Per2 in the Rat Ovary.

J. Fahrenkrug, B. Georg, J. Hannibal, P. Hindersson, and S. Gras (2006)
Endocrinology 147, 3769-3776
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Posttranslational regulation of the mammalian circadian clock by cryptochrome and protein phosphatase 5.

C. L. Partch, K. F. Shields, C. L. Thompson, C. P. Selby, and A. Sancar (2006)
PNAS 103, 10467-10472
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Development of a Two-Dimension Manifold to Represent High Dimension Mathematical Models of the Intracellular Mammalian Circadian Clock.

P. Indic, K. Gurdziel, R. E. Kronauer, and E. B. Klerman (2006)
J Biol Rhythms 21, 222-232
 |  Abstract »  |  PDF »

Twenty-Four-Hour Rhythmic Gene Expression in the Rhesus Macaque Adrenal Gland.

D. R. Lemos, J. L. Downs, and H. F. Urbanski (2006)
Mol. Endocrinol. 20, 1164-1176
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Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora..

M. Brunner and T. Schafmeier (2006)
Genes & Dev. 20, 1061-1074
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Anatomical and functional characterization of clock gene expression in neuroendocrine dopaminergic neurons.

M. T. Sellix, M. Egli, M. O. Poletini, D. T. McKee, M. D. Bosworth, C. A. Fitch, and M. E. Freeman (2006)
Am J Physiol Regulatory Integrative Comp Physiol 290, R1309-R1323
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The expression of the clock protein PER2 in the limbic forebrain is modulated by the estrous cycle.

J. S. Perrin, L. A. Segall, V. L. Harbour, B. Woodside, and S. Amir (2006)
PNAS 103, 5591-5596
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Expression of Clock and Clock-Driven Genes in the Rat Suprachiasmatic Nucleus during Late Fetal and Early Postnatal Development.

Z. Kovacikova, M. Sladek, Z. Bendova, H. Illnerova, and A. Sumova (2006)
J Biol Rhythms 21, 140-148
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Characterization of peripheral circadian clocks in adipose tissues..

S. Zvonic, A. A. Ptitsyn, S. A. Conrad, L. K. Scott, Z. E. Floyd, G. Kilroy, X. Wu, B. C. Goh, R. L. Mynatt, and J. M. Gimble (2006)
Diabetes 55, 962-970
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Functional Evolution of the Photolyase/Cryptochrome Protein Family: Importance of the C Terminus of Mammalian CRY1 for Circadian Core Oscillator Performance.

I. Chaves, K. Yagita, S. Barnhoorn, H. Okamura, G. T. J. van der Horst, and F. Tamanini (2006)
Mol. Cell. Biol. 26, 1743-1753
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Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock..

L. Yin, J. Wang, P. S. Klein, and M. A. Lazar (2006)
Science 311, 1002-1005
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