Brain-specific rescue of Clock reveals system-driven transcriptional rhythms in peripheral tissue

PLoS Genetics

Volumn 8, Issue 7, 2012, Pages

  Hughes, Michael E ^a   Hong, Hee Kyung ^b,c   Chong, Jason L ^b,c,d   Indacochea, Alejandra A ^b   Lee, Samuel S ^b   Han, Michael ^b,d   Takahashi, Joseph S ^e,f   Hogenesch, John B ^g  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

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

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

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOXYCYCLINE; PROTEIN BMAL1; RNA; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME;

ALLELE; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC MANIPULATION; GENETIC TRANSCRIPTION; LOCOMOTION; LOSS OF FUNCTION MUTATION; MALE; MICROARRAY ANALYSIS; MOLECULAR CLOCK; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUPRACHIASMATIC NUCLEUS; TRANSGENE; WILD TYPE;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; CLOCK PROTEINS; DARKNESS; GENE EXPRESSION REGULATION; LIGHT; LIVER; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, MUTANT STRAINS; ORGAN SPECIFICITY; PERIODICITY; SUPRACHIASMATIC NUCLEUS; TRANSCRIPTION, GENETIC;

ANIMALIA; MUS;

EID: 84864584460     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002835     Document Type: Article

References (61)

1. Wijnen H, Young MW, (2006) Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet 40: 409-448 doi:10.1146/annurev.genet.40.110405.090603.
2. Andretic R, Franken P, Tafti M, (2008) Genetics of sleep. Annu Rev Genet 42: 361-388 doi:10.1146/annurev.genet.42.110807.091541.
3. Dunlap JC, (1999) Molecular bases for circadian clocks. Cell 96: 271-290.
4. Harmer SL, (2009) The circadian system in higher plants. Annu Rev Plant Biol 60: 357-377 doi:10.1146/annurev.arplant.043008.092054.
5. Klerman EB, (2005) Clinical aspects of human circadian rhythms. J Biol Rhythms 20: 375-386 doi:10.1177/0748730405278353.
6. Curtis AM, Fitzgerald GA, (2006) Central and peripheral clocks in cardiovascular and metabolic function. Ann Med 38: 552-559.
7. Halberg F, Cornélissen G, Ulmer W, Blank M, Hrushesky W, et al. (2006) Cancer chronomics III. Chronomics for cancer, aging, melatonin and experimental therapeutics researchers. J Exp Ther Oncol 6: 73-84.
8. Levi F, Schibler U, (2007) Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 47: 593-628 doi:10.1146/annurev.pharmtox.47.120505.105208.
9. Ko CH, Takahashi JS, (2006) Molecular components of the mammalian circadian clock. Hum Mol Genet 15 Spec No 2: R271-277 doi:10.1093/hmg/ddl207.
10. DeBruyne JP, Weaver DR, Reppert SM, (2007) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10: 543-545 doi:10.1038/nn1884.
11. Debruyne JP, (2008) Oscillating perceptions: the ups and downs of the CLOCK protein in the mouse circadian system. J Genet 87: 437-446.
12. Yin L, Lazar MA, (2005) The orphan nuclear receptor Rev-erbalpha recruits the N-CoR/histone deacetylase 3 corepressor to regulate the circadian Bmal1 gene. Mol Endocrinol 19: 1452-1459 doi:10.1210/me.2005-0057.
13. Hastings MH, Reddy AB, Maywood ES, (2003) A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4: 649-661 doi:10.1038/nrn1177.
14. Schibler U, Sassone-Corsi P, (2002) A web of circadian pacemakers. Cell 111: 919-922.
15. Stratmann M, Schibler U, (2006) Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms 21: 494-506 doi:10.1177/0748730406293889.
16. Yu W, Hardin PE, (2006) Circadian oscillators of Drosophila and mammals. J Cell Sci 119: 4793-4795 doi:10.1242/jcs.03174.
17. Allada R, Chung BY, (2010) Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72: 605-624 doi:10.1146/annurev-physiol-021909-135815.
18. Hughes M, Deharo L, Pulivarthy SR, Gu J, Hayes K, et al. (2007) High-resolution time course analysis of gene expression from pituitary. Cold Spring Harb Symp Quant Biol 72: 381-386 doi:10.1101/sqb.2007.72.011.
19. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, et al. (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5: e1000442 doi:10.1371/journal.pgen.1000442.
20. Storch K-F, Lipan O, Leykin I, Viswanathan N, Davis FC, et al. (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83 doi:10.1038/nature744.
21. Kornmann B, Schaad O, Bujard H, Takahashi JS, Schibler U, (2007) System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 5: e34 doi:10.1371/journal.pbio.0050034.
22. Xu K, Diangelo JR, Hughes ME, Hogenesch JB, Sehgal A, (2011) The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metab 13: 639-654 doi:10.1016/j.cmet.2011.05.001.
23. McDonald MJ, Rosbash M, (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107: 567-578.
24. Lin Y, Han M, Shimada B, Wang L, Gibler TM, et al. (2002) Influence of the period-dependent circadian clock on diurnal, circadian, and aperiodic gene expression in Drosophila melanogaster. Proceedings of the National Academy of Sciences 99: 9562-9567 doi:10.1073/pnas.132269699.
25. Ueda HR, Matsumoto A, Kawamura M, Iino M, Tanimura T, et al. (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem 277: 14048-14052 doi:10.1074/jbc.C100765200.
26. Ceriani MF, Hogenesch JB, Yanovsky M, Panda S, Straume M, et al. (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22: 9305-9319.
27. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, et al. (2001) Circadian regulation of gene expression systems in the Drosophila head. Neuron 32: 657-671.
28. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, et al. (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109: 307-320.
29. Miller BH, McDearmon EL, Panda S, Hayes KR, Zhang J, et al. (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci U S A 104: 3342-3347 doi:10.1073/pnas.0611724104.
30. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, et al. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
31. Storch K-F, Paz C, Signorovitch J, Raviola E, Pawlyk B, et al. (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130: 730-741 doi:10.1016/j.cell.2007.06.045.
32. Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, et al. (2002) Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells. Curr Biol 12: 551-557.
33. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, et al. (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12: 540-550.
34. Gossen M, Freundlieb S, Bender G, Müller G, Hillen W, et al. (1995) Transcriptional activation by tetracyclines in mammalian cells. Science 268: 1766-1769.
35. Gossen M, Bujard H, (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A 89: 5547-5551.
36. Hong H-K, Chong JL, Song W, Song EJ, Jyawook AA, et al. (2007) Inducible and reversible Clock gene expression in brain using the tTA system for the study of circadian behavior. PLoS Genet 3: e33 doi:10.1371/journal.pgen.0030033.
37. Hughes ME, Hogenesch JB, Kornacker K, (2010) JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 25: 372-380 doi:10.1177/0748730410379711.
38. Schönig K, Bujard H, (2003) Generating conditional mouse mutants via tetracycline-controlled gene expression. Methods Mol Biol 209: 69-104.
39. Mahata SK, Mahata M, Marksteiner J, Sperk G, Fischer-Colbrie R, et al. (1991) Distribution of mRNAs for Chromogranins A and B and Secretogranin II in Rat Brain. Eur J Neurosci 3: 895-904.
40. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, et al. (1994) Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264: 719-725.
41. King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, et al. (1997) Positional cloning of the mouse circadian clock gene. Cell 89: 641-653.
42. Oishi K, Miyazaki K, Ishida N, (2002) Functional CLOCK is not involved in the entrainment of peripheral clocks to the restricted feeding: entrainable expression of mPer2 and BMAL1 mRNAs in the heart of Clock mutant mice on Jcl:ICR background. Biochem Biophys Res Commun 298: 198-202.
43. Ochi M, Sono S, Sei H, Oishi K, Kobayashi H, et al. (2003) Sex difference in circadian period of body temperature in Clock mutant mice with Jcl/ICR background. Neurosci Lett 347: 163-166.
44. Kennaway DJ, Varcoe TJ, Mau VJ, (2003) Rhythmic expression of clock and clock-controlled genes in the rat oviduct. Mol Hum Reprod 9: 503-507.
45. Antoch MP, Song EJ, Chang AM, Vitaterna MH, Zhao Y, et al. (1997) Functional identification of the mouse circadian Clock gene by transgenic BAC rescue. Cell 89: 655-667.
46. Atwood A, DeConde R, Wang SS, Mockler TC, Sabir JSM, et al. (2011) Cell-autonomous circadian clock of hepatocytes drives rhythms in transcription and polyamine synthesis. Proc Natl Acad Sci U S A 108: 18560-18565 doi:10.1073/pnas.1115753108.
47. Keegan KP, Pradhan S, Wang J-P, Allada R, (2007) Meta-analysis of Drosophila circadian microarray studies identifies a novel set of rhythmically expressed genes. PLoS Comput Biol 3: e208 doi:10.1371/journal.pcbi.0030208.
48. Wijnen H, Naef F, Boothroyd C, Claridge-Chang A, Young MW, (2006) Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet 2: e39 doi:10.1371/journal.pgen.0020039.
49. Rey G, Cesbron F, Rougemont J, Reinke H, Brunner M, et al. (2011) Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol 9: e1000595 doi:10.1371/journal.pbio.1000595.
50. Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornmann B, et al. (2009) REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 7: e1000181 doi:10.1371/journal.pbio.1000181.
51. Scoma HD, Humby M, Yadav G, Zhang Q, Fogerty J, et al. (2011) The de-ubiquitinylating enzyme, USP2, is associated with the circadian clockwork and regulates its sensitivity to light. PLoS ONE 6: e25382 doi:10.1371/journal.pone.0025382.
52. Oishi K, Miyazaki K, Kadota K, Kikuno R, Nagase T, et al. (2003) Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes. J Biol Chem 278: 41519-41527 doi:10.1074/jbc.M304564200.
53. Huang DW, Sherman BT, Lempicki RA, (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocols 4: 44-57 doi:10.1038/nprot.2008.211.
54. Kaasik K, Lee CC, (2004) Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature 430: 467-471 doi:10.1038/nature02724.
55. Angers M, Uldry M, Kong D, Gimble JM, Jetten AM, (2008) Mfsd2a encodes a novel major facilitator superfamily domain-containing protein highly induced in brown adipose tissue during fasting and adaptive thermogenesis. Biochem J 416: 347-355 doi:10.1042/BJ20080165.
56. Cretenet G, Le Clech M, Gachon F, (2010) Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab 11: 47-57 doi:10.1016/j.cmet.2009.11.002.
57. Kennedy D, Norman C, (2005) What Don't We Know? Science 309: 75 doi:10.1126/science.309.5731.75.
58. Pando MP, Morse D, Cermakian N, Sassone-Corsi P, (2002) Phenotypic rescue of a peripheral clock genetic defect via SCN hierarchical dominance. Cell 110: 107-117.
59. Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, et al. (2007) Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129: 605-616 doi:10.1016/j.cell.2007.02.047.
60. Welsh DK, Takahashi JS, Kay SA, (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72: 551-577 doi:10.1146/annurev-physiol-021909-135919.
61. Miyazaki M, Schroder E, Edelmann SE, Hughes ME, Kornacker K, et al. (2011) Age-Associated Disruption of Molecular Clock Expression in Skeletal Muscle of the Spontaneously Hypertensive Rat. PLoS ONE 6: e27168 doi:10.1371/journal.pone.0027168.