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Molecular Biology Reports

, Volume 39, Issue 10, pp 9783–9789 | Cite as

Differential responses of peripheral circadian clocks to a short-term feeding stimulus

  • Tao Wu
  • Ou Fu
  • Ling Yao
  • Lu Sun
  • Fen ZhuGe
  • Zhengwei Fu
Article

Abstract

To investigate the effects of a short-term feeding stimulus on the expression of circadian genes in peripheral tissues, we examined the effects of a 30-min feeding stimulus on the rapid responses and circadian phases of five clock genes (Bmal1, Cry1, Per1, Per2 and Per3) and a clock-controlled gene (Dbp) in the heart and kidney of rats. A 30 min feeding stimulus was sufficient to alter the transcript levels and circadian phases of peripheral clock genes in a tissue-specific manner. The transcript levels of most clock genes (Bmal1, Cry1, Per1, and Per2) were significantly down-regulated in the heart within 2 h, which were affected marginally in the kidney (except Per1). In addition to the rapid response of clock gene expression, we found that the circadian phases of these clock genes were markedly shifted by the 30-min feeding stimulus in the heart within 1 day. However, the same feeding stimulus almost not affected the peak phases of these clock genes in the kidney. Moreover, these differential responses of peripheral clocks to the 30-min feeding were also similarly reflected in the expression of circadian output gene Dbp. Therefore, a 30-min feeding stimulus was sufficient to induce dyssynchronized peripheral circadian rhythm and might further result in disordered downstream physiological function in rats.

Keywords

Short-term feeding Peripheral clocks Clock genes Kidney Heart 

Notes

Acknowledgments

This work was supported by a grant from the National Natural Science Foundation of China (no. 30970364), the Natural Science Foundation of Zhejiang Province, China (no. Y3090563), the Program for Changjiang Scholars and Innovative Research Team in University (no. IRT 0653).

Conflict of interest

The authors report no conflicts of interest.

References

  1. 1.
    Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549PubMedCrossRefGoogle Scholar
  2. 2.
    Schibler U, Sassone-Corsi P (2002) A web of circadian pacemakers. Cell 111:919–922PubMedCrossRefGoogle Scholar
  3. 3.
    Shigeyoshi Y, Taguchi K, Yamamoto S, Takekida S, Yan L, Tei H, Moriya T, Shibata S, Loros JJ, Dunlap JC, Okamura H (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91:1043–1053PubMedCrossRefGoogle Scholar
  4. 4.
    Cuninkova L, Brown SA (2008) Peripheral circadian oscillators: interesting mechanisms and powerful tools. Ann NY Acad Sci 1129:358–370PubMedCrossRefGoogle Scholar
  5. 5.
    Suter DM, Schibler U (2009) Physiology. Feeding the clock. Science 326:378–379PubMedCrossRefGoogle Scholar
  6. 6.
    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 14:2950–2961PubMedCrossRefGoogle Scholar
  7. 7.
    Hara R, Wan K, Wakamatsu H, Aida R, Moriya T, Akiyama M, Shibata S (2001) Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells 6:269–278PubMedCrossRefGoogle Scholar
  8. 8.
    Minana-Solis MC, Angeles-Castellanos M, Feillet C, Pevet P, Challet E, Escobar C (2009) Differential effects of a restricted feeding schedule on clock-gene expression in the hypothalamus of the rat. Chronobiol Int 26:808–820PubMedCrossRefGoogle Scholar
  9. 9.
    Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490–493PubMedCrossRefGoogle Scholar
  10. 10.
    Wu T, Ni Y, Kato H, Fu Z (2010) Feeding-induced rapid resetting of the hepatic circadian clock is associated with acute induction of Per2 and Dec1 transcription in rats. Chronobiol Int 27:1–18PubMedCrossRefGoogle Scholar
  11. 11.
    Lamia KA, Storch KF, Weitz CJ (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA 105:15172–15177PubMedCrossRefGoogle Scholar
  12. 12.
    Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornmann B, Sasso GL, Moschetta A, Schibler U (2009) REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 7:e1000181PubMedCrossRefGoogle Scholar
  13. 13.
    Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U (2004) The mammalian circadian timing system: from gene expression to physiology. Chromosoma 113:103–112PubMedCrossRefGoogle Scholar
  14. 14.
    Yamajuku D, Okubo S, Haruma T, Inagaki T, Okuda Y, Kojima T, Noutomi K, Hashimoto S, Oda H (2009) Regular feeding plays an important role in cholesterol homeostasis through the liver circadian clock. Circ Res 105:545–548PubMedCrossRefGoogle Scholar
  15. 15.
    Salgado-Delgado R, Angeles-Castellanos M, Saderi N, Buijs RM, Escobar C (2010) Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology 151:1019–1029PubMedCrossRefGoogle Scholar
  16. 16.
    Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935–941PubMedCrossRefGoogle Scholar
  17. 17.
    Wu T, Jin Y, Ni Y, Zhang D, Kato H, Fu Z (2008) Effects of light cues on re-entrainment of the food-dominated peripheral clocks in mammals. Gene 419:27–34PubMedCrossRefGoogle Scholar
  18. 18.
    Portaluppi F, Touitou Y, Smolensky MH (2008) Ethical and methodological standards for laboratory and medical biological rhythm research. Chronobiol Int 25:999–1016PubMedCrossRefGoogle Scholar
  19. 19.
    Wu T, Jin Y, Kato H, Fu Z (2008) Light and food signals cooperate to entrain the rat pineal circadian system. J Neurosci Res 86:3246–3255PubMedCrossRefGoogle Scholar
  20. 20.
    Oike H, Nagai K, Fukushima T, Ishida N, Kobori M (2011) Feeding cues and injected nutrients induce acute expression of multiple clock genes in the mouse liver. PLoS One 6:e23709PubMedCrossRefGoogle Scholar
  21. 21.
    Wu T, Ni Y, Dong Y, Xu J, Song X, Kato H, Fu Z (2010) Regulation of circadian gene expression in the kidney by light and food cues in rats. Am J Physiol Regul Integr Comp Physiol 298:R635–R641PubMedCrossRefGoogle Scholar
  22. 22.
    Kawamoto T, Noshiro M, Furukawa M, Honda KK, Nakashima A, Ueshima T, Usui E, Katsura Y, Fujimoto K, Honma S, Honma K, Hamada T, Kato Y (2006) Effects of fasting and re-feeding on the expression of Dec1, Per1, and other clock-related genes. J Biochem 140:401–408PubMedCrossRefGoogle Scholar
  23. 23.
    Mistlberger RE (2006) Circadian rhythms: perturbing a food-entrained clock. Curr Biol 16:R968–R969PubMedCrossRefGoogle Scholar
  24. 24.
    Mistlberger RE (2011) Neurobiology of food anticipatory circadian rhythms. Physiol Behav 104:535–545PubMedCrossRefGoogle Scholar
  25. 25.
    Mistlberger RE, Antle MC (2011) Entrainment of circadian clocks in mammals by arousal and food. Essays Biochem 49:119–136PubMedGoogle Scholar
  26. 26.
    Dudley CA, Erbel-Sieler C, Estill SJ, Reick M, Franken P, Pitts S, McKnight SL (2003) Altered patterns of sleep and behavioral adaptability in NPAS2-deficient mice. Science 301:379–383PubMedCrossRefGoogle Scholar
  27. 27.
    Hirota T, Okano T, Kokame K, Shirotani-Ikejima H, Miyata T, Fukada Y (2002) Glucose down-regulates Per1 and Per2 mRNA levels and induces circadian gene expression in cultured Rat-1 fibroblasts. J Biol Chem 277:44244–44251PubMedCrossRefGoogle Scholar
  28. 28.
    Rutter J, Reick M, Wu LC, McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293:510–514PubMedCrossRefGoogle Scholar
  29. 29.
    Davidson AJ, Stephan FK (1999) Plasma glucagon, glucose, insulin, and motilin in rats anticipating daily meals. Physiol Behav 66:309–315PubMedCrossRefGoogle Scholar
  30. 30.
    Green CB, Takahashi JS, Bass J (2008) The meter of metabolism. Cell 134:728–742PubMedCrossRefGoogle Scholar
  31. 31.
    Wu T, Sun L, Zhuge F, Guo X, Zhao Z, Tang R, Chen Q, Chen L, Kato H, Fu Z (2011) Differential roles of breakfast and supper in rats of a daily three-meal schedule upon circadian regulation and physiology. Chronobiol Int 28:890–903PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Tao Wu
    • 1
  • Ou Fu
    • 2
  • Ling Yao
    • 1
  • Lu Sun
    • 1
  • Fen ZhuGe
    • 1
  • Zhengwei Fu
    • 1
  1. 1.College of Biological and Environmental EngineeringZhejiang University of TechnologyHangzhouChina
  2. 2.College of Animal SciencesZhejiang UniversityHangzhouChina

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