Real-time recording of circadian liver gene expression in freely moving mice reveals the phase-setting behavior of hepatocyte clocks

Genes and Development

Volumn 27, Issue 13, 2013, Pages 1526-1536

  Saini, Camille ^a,b   Liani, André ^a,b   Curie, Thomas ^c   Gos, Pascal ^a,b   Kreppel, Florian ^d   Emmenegger, Yann ^c   Bonacina, Luigi ^a   Wolf, Jean Pierre ^a   Poget, Yves Alain ^a,b   Franken, Paul ^c   Schibler, Ueli ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b National Centre of Competence in Research Frontiers in Genetics   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

Circadian gene expression; Liver oscillators; Real time bioluminescence monitoring; Resetting cues; SCN lesion

Indexed keywords

LUCIFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLUMINESCENCE; CELL FUNCTION; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE EXPRESSION; LIVER CELL; MALE; MOUSE; NONHUMAN; OSCILLATOR; PHOTON; PRIORITY JOURNAL; REPORTER GENE; SUPRACHIASMATIC NUCLEUS;

CIRCADIAN GENE EXPRESSION; LIVER OSCILLATORS; REAL-TIME BIOLUMINESCENCE MONITORING; RESETTING CUES; SCN LESION;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HEPATOCYTES; LIVER; LUMINESCENT MEASUREMENTS; MALE; MICE; MICE, HAIRLESS; MOTOR ACTIVITY; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS;

MUS;

EID: 84879773624     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.221374.113     Document Type: Article

References (49)

1. Abel J, Haarmann-Stemmann T. 2010. An introduction to the molecular basics of aryl hydrocarbon receptor biology. Biol Chem 391: 1235-1248.
2. Alba R, Bradshaw AC, Parker AL, Bhella D, Waddington SN, Nicklin SA, van Rooijen N, Custers J, Goudsmit J, Barouch DH, et al. 2009. Identification of coagulation factor (F)X binding sites on the adenovirus serotype 5 hexon: Effect of mutagenesis on FX interactions and gene transfer. Blood 114: 965-971.
3. Albrecht U, Zheng B, Larkin D, Sun ZS, Lee CC. 2001. MPer1 and mper2 are essential for normal resetting of the circadian clock. J Biol Rhythms 16: 100-104.
4. Altucci L, Leibowitz MD, Ogilvie KM, de Lera AR, Gronemeyer H. 2007. RAR and RXR modulation in cancer and metabolic disease. Nat Rev Drug Discov 6: 793-810.
5. Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, Mostoslavsky R, Alt FW, Schibler U. 2008. SIRT1 regulates circadian clock gene expression through PER2 deacetylation. Cell 134: 317-328.
6. Asher G, Reinke H, Altmeyer M, Gutierrez-Arcelus M, Hottiger MO, Schibler U. 2010. Poly(ADP-ribose) polymerase 1 participates in the phase entrainment of circadian clocks to feeding. Cell 142: 943-953.
7. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U. 2000. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289: 2344-2347.
8. Bradshaw AC, Parker AL, Duffy MR, Coughlan L, van Rooijen N, Kahari VM, Nicklin SA, Baker AH. 2010. Requirements for receptor engagement during infection by adenovirus complexed with blood coagulation factor X. PLoS Pathog 6: e1001142.
9. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U. 2002. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12: 1574-1583.
10. Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F, Jager J, Lazar MA. 2012. Rev-erba and Rev-erbb coordinately protect the circadian clock and normal metabolic function. Genes Dev 26: 657-667.
11. Buhr ED, Yoo SH, Takahashi JS. 2010. Temperature as a universal resetting cue for mammalian circadian oscillators. Science 330: 379-385.
12. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, et al. 2012. Regulation of circadian behaviour and metabolism by REV-ERB-a and REV-ERB-b. Nature 485: 123-127.
13. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. 2000. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14: 2950-2961.
14. Dibner C, Schibler U, Albrecht U. 2010. Themammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annu Rev Physiol 72: 517-549.
15. Duffy MR, Bradshaw AC, Parker AL, McVey JH, Baker AH. 2011. A cluster of basic amino acids in the factor X serine protease mediates surface attachment of adenovirus/FX complexes. J Virol 85: 10914-10919.
16. Grimaldi PA. 2007. Peroxisome proliferator-activated receptors as sensors of fatty acids and derivatives. Cell Mol Life Sci 64: 2459-2464.
17. Guo H, Brewer JM, Lehman MN, Bittman EL. 2006. Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: Effects of transplanting the pacemaker. J Neurosci 26: 6406-6412.
18. Handschin C, Meyer UA. 2005. Regulatory network of lipidsensing nuclear receptors: Roles for CAR, PXR, LXR, and FXR. Arch Biochem Biophys 433: 387-396.
19. Hoffman RM, Yang M. 2006. Whole-body imaging with fluorescent proteins. Nat Protoc 1: 1429-1438.
20. Jetten AM. 2009. Retinoid-related orphan receptors (RORs): Critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl Recept Signal 7: e003.
21. Kaelin WG Jr, Ratcliffe PJ. 2008. Oxygen sensing by metazoans: The central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402.
22. 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.
23. Kreppel F, Biermann V, Kochanek S, Schiedner G. 2002. A DNAbased method to assay total and infectious particle contents and helper virus contamination in high-capacity adenoviral vector preparations. Hum Gene Ther 13: 1151-1156.
24. Kuipers F, Stroeve JH, Caron S, Staels B. 2007. Bile acids, farnesoid X receptor, atherosclerosis and metabolic control. Curr Opin Lipidol 18: 289-297.
25. Le Minh N, Damiola F, Tronche F, Schutz G, Schibler U. 2001. Glucocorticoid hormones inhibit food-induced phase-shifting of peripheral circadian oscillators. EMBO J 20: 7128-7136.
26. McPherson R, Gauthier A. 2004. Molecular regulation of SREBP function: The Insig-SCAP connection and isoform-specific modulation of lipid synthesis. Biochem Cell Biol 82: 201-211.
27. Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U. 2004. Circadian gene expression in individual fibroblasts: Cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 119: 693-705.
28. Oishi K, Fukui H, Sakamoto K, Miyazaki K, Kobayashi H, Ishida N. 2002. Differential expressions of mPer1 and mPer2 mRNAs under a skeleton photoperiod and a complete light-dark cycle. Brain Res Mol Brain Res 109: 11-17.
29. Peraza MA, Burdick AD, Marin HE, Gonzalez FJ, Peters JM. 2006. The toxicology of ligands for peroxisome proliferatoractivated receptors (PPAR). Toxicol Sci 90: 269-295.
30. Postic C, Dentin R, Denechaud PD, Girard J. 2007. ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr 27: 179-192.
31. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U. 2002. The orphan nuclear receptor REV-ERBa controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110: 251-260.
32. Prill JM, Espenlaub S, Samen U, Engler T, Schmidt E, Vetrini F, Rosewell A, Grove N, Palmer D, Ng P, et al. 2011. Modifications of adenovirus hexon allow for either hepatocyte detargeting or targeting with potential evasion from Kupffer cells. Mol Ther 19: 83-92.
33. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, Gonzalez FJ, Lilley KS, Kyriacou CP, Hastings MH. 2007. Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45: 1478-1488.
34. Reinke H, Saini C, Fleury-Olela F, Dibner C, Benjamin IJ, Schibler U. 2008. Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22: 331-345.
35. Relogio A, Westermark PO, Wallach T, Schellenberg K, Kramer A, Herzel H. 2011. Tuning the mammalian circadian clock: Robust synergy of two loops. PLoS Comput Biol 7: e1002309.
36. Saini C, Morf J, Stratmann M, Gos P, Schibler U. 2012. Simulated body temperature rhythms reveal the phase-shifting behavior and plasticity of mammalian circadian oscillators. Genes Dev 26: 567-580.
37. Sandhu GS, Solorio L, Broome AM, Salem N, Kolthammer J, Shah T, Flask C, Duerk JL. 2010. Whole animal imaging. Wiley Interdiscip Rev Syst Biol Med 2: 398-421.
38. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. 2001. Entrainment of the circadian clock in the liver by feeding. Science 291: 490-493.
39. Stratmann M, Schibler U. 2006. Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms 21: 494-506.
40. Stratmann M, Stadler F, Tamanini F, van der Horst GT, Ripperger JA. 2010. Flexible phase adjustment of circadian albumin D site-binding protein (DBP) gene expression by CRYPTOCHROME1. Genes Dev 24: 1317-1328.
41. Tahara Y, Kuroda H, Saito K, Nakajima Y, Kubo Y, Ohnishi N, Seo Y, Otsuka M, Fuse Y, Ohura Y, et al. 2012. In vivo monitoring of peripheral circadian clocks in the mouse. Curr Biol 22: 1029-1034.
42. Takeda Y, Kang HS, Angers M, Jetten AM. 2011. Retinoic acidrelated orphan receptor g directly regulates neuronal PAS domain protein 2 transcription in vivo. Nucleic Acids Res 39: 4769-4782.
43. Tan NS, Michalik L, Desvergne B, Wahli W. 2005. Multiple expression control mechanisms of peroxisome proliferatoractivated receptors and their target genes. J Steroid Biochem Mol Biol 93: 99-105.
44. van der Veen DR, Minh NL, Gos P, Arneric M, Gerkema MP, Schibler U. 2006. Impact of behavior on central and peripheral circadian clocks in the common vole Microtus arvalis, a mammal with ultradian rhythms. Proc Natl Acad Sci 103: 3393-3398.
45. Vujovic N, Davidson AJ, Menaker M. 2008. Sympathetic input modulates, but does not determine, phase of peripheral circadian oscillators. Am J Physiol Regul Integr Comp Physiol 295: R355-R360.
46. Waddington SN, McVey JH, Bhella D, Parker AL, Barker K, Atoda H, Pink R, Buckley SM, Greig JA, Denby L, et al. 2008. Adenovirus serotype 5 hexon mediates liver gene transfer. Cell 132: 397-409.
47. Yamaguchi S, Kobayashi M, Mitsui S, Ishida Y, van der Horst GT, Suzuki M, Shibata S, Okamura H. 2001. View of a mouse clock gene ticking. Nature 409: 684.
48. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. 2000. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288: 682-685.
49. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, et al. 2004. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci 101: 5339-5346.