Molecular architecture of the mammalian circadian clock

Trends in Cell Biology

Volumn 24, Issue 2, 2014, Pages 90-99

  Partch, Carrie L ^a,b   Green, Carla B ^c   Takahashi, Joseph S ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Circadian; Peripheral clock; Post transcription; Transcription

Indexed keywords

RNA POLYMERASE II;

BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; MAMMAL; MOLECULAR CLOCK; NONHUMAN; PHYSIOLOGY; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; REVIEW; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

MAMMALIA;

CIRCADIAN; PERIPHERAL CLOCK; POST-TRANSCRIPTION; TRANSCRIPTION;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; HUMANS;

EID: 84892976423     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2013.07.002     Document Type: Review

References (115)

1. Lowrey P., Takahashi J. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu. Rev. Genomics Hum. Genet. 2004, 5:407-441.
2. Kang T.H., et al. Circadian oscillation of nucleotide excision repair in mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2864-2867.
3. Kang T-H., et al. Circadian control of XPA and excision repair of cisplatin-DNA damage by cryptochrome and HERC2 ubiquitin ligase. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4890-4895.
4. Ko C., Takahashi J. Molecular components of the mammalian circadian clock. Hum. Mol. Genet. 2006, 15(Special issue 2):7.
5. Mohawk J., Takahashi J. Cell autonomy and synchrony of suprachiasmatic nucleus circadian oscillators. Trends Neurosci. 2011, 34:349-358.
6. Buhr E., et al. Temperature as a universal resetting cue for mammalian circadian oscillators. Science 2010, 330:379-385.
7. Dibner C., et al. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 2010, 72:517-549.
8. Yoo S-H., et al. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:5339-5346.
9. Liu A., et al. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 2007, 129:605-616.
10. Ralph M., et al. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990, 247:975-978.
11. Yang X., et al. Nuclear receptors, metabolism, and the circadian clock. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:387-394.
12. Brown S., et al. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr. Biol. 2002, 12:1574-1583.
13. Saini C., et al. Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev. 2012, 26:567-580.
14. Stratmann M., Schibler U. Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J. Biol. Rhythms 2006, 21:494-506.
15. Cho H., et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 2012, 485:123-127.
16. DeBruyne J., et al. CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat. Neurosci. 2007, 10:543-545.
17. Liu A., et al. Redundant function of REV-ERBalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet. 2008, 4:e1000023.
18. Bae K., et al. Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 2001, 30:525-536.
19. Lee Y., et al. Stoichiometric relationship among clock proteins determines robustness of circadian rhythms. J. Biol. Chem. 2011, 286:7033-7042.
20. Kondratov R., et al. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 2006, 20:1868-1873.
21. McDearmon E., et al. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science 2006, 314:1304-1308.
22. Sun Y., et al. The mortality of MOP3 deficient mice with a systemic functional failure. J. Biomed. Sci. 2006, 13:845-851.
23. Cheng B., et al. Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:17147-17152.
24. Lamia K., et al. Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:15172-15177.
25. Marcheva B., et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010, 466:627-631.
26. Storch K-F., et al. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 2007, 130:730-741.
27. Kornmann B., et al. System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 2007, 5:e34.
28. Miller B., et al. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3342-3347.
29. Panda S., et al. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002, 109:307-320.
30. Storch K-F., et al. Extensive and divergent circadian gene expression in liver and heart. Nature 2002, 417:78-83.
31. Gachon F., et al. The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab. 2006, 4:25-36.
32. Preitner N., et al. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002, 110:251-260.
33. Hamaguchi H., et al. Expression of the gene for Dec2, a basic helix-loop-helix transcription factor, is regulated by a molecular clock system. Biochem. J. 2004, 382:43-50.
34. Reddy A., et al. Circadian orchestration of the hepatic proteome. Curr. Biol. 2006, 16:1107-1115.
35. Kojima S., et al. Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 2012, 26:2724-2736.
36. McGlincy N., et al. Regulation of alternative splicing by the circadian clock and food related cues. Genome Biol. 2012, 13:R54.
37. Feng D., et al. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 2011, 331:1315-1319.
38. Hatanaka F., et al. Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. Mol. Cell. Biol. 2010, 30:5636-5648.
39. Koike N., et al. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012, 338:349-354.
40. Le Martelot G., et al. Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS Biol. 2012, 10:e1001442.
41. Menet J., et al. Nascent-Seq reveals novel features of mouse circadian transcriptional regulation. eLife 2012, 1:e00011.
42. Rey G., et al. Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol. 2011, 9:e1000595.
43. Vollmers C., et al. Circadian oscillations of protein-coding and regulatory RNAs in a highly dynamic mammalian liver epigenome. Cell Metab. 2012, 16:833-845.
44. Brown S., et al. (Re)inventing the circadian feedback loop. Dev. Cell 2012, 22:477-487.
45. Lamia K., et al. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 2011, 480:552-556.
46. Schmutz I., et al. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev. 2010, 24:345-357.
47. Chen R., et al. Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol. Cell 2009, 36:417-430.
48. Lee H-M., et al. The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:16451-16456.
49. Brown S., et al. PERIOD1-associated proteins modulate the negative limb of the mammalian circadian oscillator. Science 2005, 308:693-696.
50. Duong H., et al. A molecular mechanism for circadian clock negative feedback. Science 2011, 332:1436-1439.
51. Kowalska E., et al. Distinct roles of DBHS family members in the circadian transcriptional feedback loop. Mol. Cell. Biol. 2012, 32:4585-4594.
52. Padmanabhan K., et al. Feedback regulation of transcriptional termination by the mammalian circadian clock PERIOD complex. Science 2012, 337:599-602.
53. Tamanini F., et al. Structure function analysis of mammalian cryptochromes. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:133-139.
54. Stratmann M., et al. Flexible phase adjustment of circadian albumin D site-binding protein (DBP) gene expression by CRYPTOCHROME1. Genes Dev. 2010, 24:1317-1328.
55. Ukai-Tadenuma M., et al. Delay in feedback repression by cryptochrome 1 is required for circadian clock function. Cell 2011, 144:268-281.
56. Khan S., et al. Identification of a novel cryptochrome differentiating domain required for feedback repression in circadian clock function. J. Biol. Chem. 2012, 287:25917-25926.
57. McCarthy E., et al. Generation of a novel allelic series of cryptochrome mutants via mutagenesis reveals residues involved in protein-protein interaction and CRY2-specific repression. Mol. Cell. Biol. 2009, 29:5465-5476.
58. Ye R., et al. Biochemical analysis of the canonical model for the mammalian circadian clock. J. Biol. Chem. 2011, 286:25891-25902.
59. Huang N., et al. Crystal structure of the heterodimeric CLOCK:BMAL1 transcriptional activator complex. Science 2012, 337:189-194.
60. Wang Z., et al. Intermolecular recognition revealed by the complex structure of human CLOCK-BMAL1 basic helix-loop-helix domains with E-box DNA. Cell Res. 2012, 2012:1-12.
61. McIntosh B., et al. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Annu. Rev. Physiol. 2010, 72:625-645.
62. Partch C., Gardner K. Coactivator recruitment: a new role for PAS domains in transcriptional regulation by the bHLH-PAS family. J. Cell. Physiol. 2010, 223:553-557.
63. Kiyohara Y., et al. The BMAL1 C terminus regulates the circadian transcription feedback loop. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10074-10079.
64. Hennig S., et al. Structural and functional analyses of PAS domain interactions of the clock proteins Drosophila PERIOD and mouse PERIOD2. PLoS Biol. 2009, 7:e94.
65. Kucera N., et al. Unwinding the differences of the mammalian PERIOD clock proteins from crystal structure to cellular function. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3311-3316.
66. Zhao W-N., et al. CIPC is a mammalian circadian clock protein without invertebrate homologues. Nat. Cell Biol. 2007, 9:268-275.
67. Czarna A., et al. Quantitative analyses of cryptochrome-mBMAL1 interactions: mechanistic insights into the transcriptional regulation of the mammalian circadian clock. J. Biol. Chem. 2011, 286:22414-22425.
68. Katada S., Sassone-Corsi P. The histone methyltransferase MLL1 permits the oscillation of circadian gene expression. Nat. Struct. Mol. Biol. 2010, 17:1414-1421.
69. Takahata S., et al. Transactivation mechanisms of mouse clock transcription factors, mClock and mArnt3. Genes Cells 2000, 5:739-747.
70. Chaves I., et al. Functional evolution of the photolyase/cryptochrome protein family: importance of the C terminus of mammalian CRY1 for circadian core oscillator performance. Mol. Cell. Biol. 2006, 26:1743-1753.
71. Ozber N., et al. Identification of two amino acids in the C-terminal domain of mouse CRY2 essential for PER2 interaction. BMC Mol. Biol. 2010, 11:69.
72. Busino L., et al. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science 2007, 316:900-904.
73. Siepka S., et al. Circadian mutant Overtime reveals F-box protein FBXL3 regulation of cryptochrome and period gene expression. Cell 2007, 129:1011-1023.
74. Czarna A., et al. Structures of Drosophila cryptochrome and mouse cryptochrome1 provide insight into circadian function. Cell 2013, 153:1394-1405.
75. Xing W., et al. SCFFBXL3 ubiquitin ligase targets cryptochromes at their cofactor pocket. Nature 2013, 496:64-68.
76. Fuda N., et al. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 2009, 461:186-192.
77. Etchegaray J-P., et al. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 2003, 421:177-182.
78. DiTacchio L., et al. Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 2011, 333:1881-1885.
79. Doi M., et al. Circadian regulator CLOCK is a histone acetyltransferase. Cell 2006, 125:497-508.
80. Etchegaray J-P., et al. The polycomb group protein EZH2 is required for mammalian circadian clock function. J. Biol. Chem. 2006, 281:21209-21215.
81. Jones M., et al. Jumonji domain protein JMJD5 functions in both the plant and human circadian systems. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21623-21628.
82. +-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell 2008, 134:329-340.
83. Masri S., et al. The circadian clock transcriptional complex: metabolic feedback intersects with epigenetic control. Ann. N. Y. Acad. Sci. 2012, 1264:103-109.
84. Raj A., van Oudenaarden A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 2008, 135:216-226.
85. Suter D., et al. Mammalian genes are transcribed with widely different bursting kinetics. Science 2011, 332:472-474.
86. Suter D., et al. Origins and consequences of transcriptional discontinuity. Curr. Opin. Cell Biol. 2011, 23:657-662.
87. Motta-Mena L., et al. The three Rs of transcription: recruit, retain, and recycle. Mol. Cell 2010, 40:855-858.
88. + salvage pathway by CLOCK-SIRT1. Science 2009, 324:654-657.
89. + biosynthesis. Science 2009, 324:651-654.
90. Asher G., et al. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 2010, 142:943-953.
91. Peek C., et al. Nutrient sensing and the circadian clock. Trends Endocrinol. Metab. 2012, 23:312-318.
92. Dibner C., et al. Circadian gene expression is resilient to large fluctuations in overall transcription rates. EMBO J. 2009, 28:123-134.
93. Morf J., et al. Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally. Science 2012, 338:379-383.
94. Baggs J., Green C. Nocturnin, a deadenylase in Xenopus laevis retina: a mechanism for posttranscriptional control of circadian-related mRNA. Curr. Biol. 2003, 13:189-198.
95. Garbarino-Pico E., et al. Immediate early response of the circadian polyA ribonuclease nocturnin to two extracellular stimuli. RNA 2007, 13:745-755.
96. Douris N., et al. Nocturnin regulates circadian trafficking of dietary lipid in intestinal enterocytes. Curr. Biol. 2011, 21:1347-1355.
97. Green C., et al. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9888-9893.
98. Hughes M., et al. Harmonics of circadian gene transcription in mammals. PLoS Genet. 2009, 5:e1000442.
99. Hughes M., et al. Brain-specific rescue of Clock reveals system-driven transcriptional rhythms in peripheral tissue. PLoS Genet. 2012, 8:e1002835.
100. Pardee K., et al. The structural basis of gas-responsive transcription by the human nuclear hormone receptor REV-ERBbeta. PLoS Biol. 2009, 7:e43.
101. Phelan C., et al. Structure of Rev-erbalpha bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat. Struct. Mol. Biol. 2010, 17:808-814.
102. Wang Z., et al. Intermolecular recognition revealed by the complex structure of human CLOCK-BMAL1 basic helix-loop-helix domains with E-box DNA. Cell Res. 2012, 23:213-223.
103. Ptácek L., et al. Novel insights from genetic and molecular characterization of the human clock. Cold Spring Harb. Symp. Quant. Biol. 2007, 72:273-277.
104. Hirota T., et al. High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIα as a clock regulatory kinase. PLoS Biol. 2010, 8:e1000559.
105. Isojima Y., et al. CKIepsilon/delta-dependent phosphorylation is a temperature-insensitive, period-determining process in the mammalian circadian clock. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15744-15749.
106. Solt L., et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 2012, 485:62-68.
107. Chen Z., et al. Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:101-106.
108. Pagani L., et al. Serum factors in older individuals change cellular clock properties. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7218-7223.
109. Godinho S., et al. The after-hours mutant reveals a role for Fbxl3 in determining mammalian circadian period. Science 2007, 316:897-900.
110. Reischl S., et al. Beta-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J. Biol. Rhythms 2007, 22:375-386.
111. Shirogane T., et al. SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem. 2005, 280:26863-26872.
112. Partch C., et al. Posttranslational regulation of the mammalian circadian clock by cryptochrome and protein phosphatase 5. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10467-10472.
113. Toh K., et al. An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 2001, 291:1040-1043.
114. Xu Y., et al. Functional consequences of a CKIdelta mutation causing familial advanced sleep phase syndrome. Nature 2005, 434:640-644.
115. Sato T., et al. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 2004, 43:527-537.