Timed hypocaloric feeding and melatonin synchronize the suprachiasmatic clockwork in rats, but with opposite timing of behavioral output

European Journal of Neuroscience

Volumn 22, Issue 4, 2005, Pages 921-929

  Caldelas, Ivette ^a,b   Feillet, Celine A ^a   Dardente, Hugues ^a,c   Eclancher, Françoise ^a   Malan, André ^a   Gourmelen, Sylviane ^a   Pévet, Paul ^a   Challet, Etienne ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Behavior; Circadian rhythm; Feeding; Gene; Melatonin; Suprachiasmatic nucleus

Indexed keywords

MELATONIN; VASOPRESSIN;

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR; BMAL1 GENE; CIRCADIAN RHYTHM; CLOCK GENE; CONTROLLED STUDY; FEEDING; GENE; GENE EXPRESSION; LIGHT DARK CYCLE; LOCOMOTION; LOW CALORY DIET; MALE; MOLECULAR CLOCK; NONHUMAN; OSCILLATION; PER1 GENE; PER2 GENE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; REST; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; WAVEFORM;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL CLOCKS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; LIGHT; MALE; MELATONIN; MOTOR ACTIVITY; RATS; RATS, WISTAR; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

EID: 24144432242     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04284.x     Document Type: Article

References (44)

1. Abe, H., Honma, S., Namihira, M., Tanahashi, Y., Ikeda, M. & Honma, K. (1998) Circadian rhythm and light responsiveness of BMAL1 expression, a partner of mammalian clock gene Clock, in the suprachiasmatic nucleus of rats. Neurosci. Lett., 258, 93-96.
2. Albrecht, U., Sun, Z.S., Eichele, G. & Lee, C.C. (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell, 91, 1055-1064.
3. Aschoff, J., Daan, S. & Honma, K.I. (1982) Zeitgebers, entrainment, and masking: some unsettled questions. In Aschoff, J., Daan, S. & Groos, G. (Eds), Vertebrate Circadian Systems. Springer-Verlag, Berlin, pp. 13-24.
4. Beaule, C. & Amir, S. (1999) Photic entrainment and induction of immediate-early genes within the rat circadian system. Brain Res., 821, 95-100.
5. Caldelas, I., Poirel, V.J., Sicard, B., Pevet, P. & Challet, E. (2003) Circadian profile and photic regulation of clock genes in the suprachiasmatic nucleus of a diurnal mammal Arvicanthis ansorgei. Neuroscience, 116, 583-591.
6. Castillo, M.R., Hochstetler, K.J., Tavernier, R.J. Jr, Greene, D.M. & Bult-Ito, A. (2004) Entrainment of the master circadian clock by scheduled feeding. Am. J. Physiol. Regul. Integr. Comp. Physiol., 287, R551-R555.
7. Challet, E., Malan, A. & Pevet, P. (1996) Daily hypocaloric feeding entrains circadian rhythms of wheel-running and body temperature in rats kept in constant darkness. Neurosci. Lett., 211, 1-4.
8. Challet, E. & Pevet, P. (2003) Interactions between photic and nonphotic stimuli to synchronize the master circadian clock in mammals. Front. Biosci., 8, S246-S257.
9. Challet, E., Pevet, P., Vivien-Roels, B. & Malan, A. (1997) Phase-advanced daily rhythms of melatonin, body temperature, locomotor activity in food-restricted rats fed during daytime. J. Biol. Rhythms, 12, 65-79.
10. 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.
11. Dardente, H., Menet, J.S., Challet, E., Tournier, B., Pevet, P. & Masson-Pevet, M. (2004) Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res. Mol. Brain Res., 124, 143-151.
12. 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, 269-278.
13. Hoogenboom, I., Daan, S., Dallinga, J.H. & Schoenmakers, M. (1984) Seasonal change in the daily timing of behavivour of the common vole, Microtus arvalis. Oecologia (Berl.), 61, 18-31.
14. Jin, X., Shearman, L.P., Weaver, D.R., Zylka, M.J., de Vries, G.J. & Reppert, S.M. (1999) A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell, 96, 57-68.
15. Kas, M.J. & Edgar, D.M. (1999) A nonphotic stimulus inverts the diurnal-nocturnal phase preference in Octodon degus. J. Neurosci., 19, 328-333.
16. Lambert, C.M., Machida, K.K., Smale, L., Nunez, A.A. & Weaver, D.R. (2005) Analysis of the Prokineticin 2 system in a diurnal rodent, the unstriped Nile rat (Arvicanthis niloticus). J. Biol. Rhythms, 20, 206-218.
17. Lamont, E.W., Renteria Diaz, L., Barry-Shaw, J., Stewart, J. & Amir, S. (2005) Daily restricted feeding rescues a rhythm of Period 2 expression in the arrhythmic suprachiasmatic nucleus. Neuroscience, 132, 245-248.
18. Lowrey, P.L. & Takahashi, J.S. (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu. Rev. Genomics Hum. Genet., 5, 407-441.
19. Maywood, E.S. & Mrosvosky, N. (2001) A molecular explanation of interactions between photic and non-photic circadian clock-resetting stimuli. Gene Ex. Patt. Brain Res., 1, 27-31.
20. Maywood, E.S., Mrosvosky, N., Field, M.D. & Hastings, M.H. (1999) Rapid down-regulation of mammalian Period genes during behavioral resetting of the circadian clock. Proc. Natl Acad. Sci. USA, 96, 15211-15216.
21. Mendoza, J., Graff, C., Dardente, H., Pevet, P. & Challet, E. (2005) Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light-dark cycle. J. Neurosci., 25, 1514-1522.
22. Mistlberger, R.E. (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev., 18, 171-195.
23. Mistlberger, R.E., de Groot, M.H.M., Bossert, J.M. & Marchant, E.G. (1996) Discrimination of circadian phase in intact and suprachiasmatic nuclei-ablated rats. Brain Res., 739, 12-18.
24. Mrosovsky, N., Edelstein, K., Hastings, M.H. & Maywood, E.S. (2001) Cycle of period gene expression in a diurnal mammal (Spermophilus tridecemlineatus): implications for nonphotic phase shifting. J. Biol. Rhythms, 16, 471-478.
25. Novak, C.M., Smale, L. & Nunez, A.A. (2000) Rhythms in Fos expression in brain areas related to the sleep-wake cycle in the diurnal Arvicanthis niloticus. Am. J. Physiol. Regul. Integr. Comp. Physiol., 278, R1267-R1274.
26. Oster, H., Avivi, A., Joel, A., Albrecht, U. & Nevo, E. (2002) A switch from diurnal to nocturnal activity in S. ehrenbergi is accompanied by an uncoupling of light input and the circadian clock. Curr. Biol., 12, 1919-1922.
27. Pitrosky, B., Kirsch, R., Malan, A., Mocaer, E. & Pevet, P. (1999) Organization of rat circadian rhythms during daily infusion of melatonin or S20098, a melatonin agonist. Am. J. Physiol. Regul. Integr. Comp. Physiol., 277, R812-R828.
28. Poirel, V.J., Boggio, V., Dardente, H., Pevet, P., Masson-Pevet, M. & Gauer, F. (2003) Contrary to other non-photic cues, acute melatonin injection does not induce immediate changes of clock gene mRNA expression in the rat suprachiasmatic nuclei. Neuroscience, 120, 745-755.
29. Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U. & Schibler, U. (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell, 110, 251-260.
30. Redlin, U. (2001) Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol. Int., 18, 737-758.
31. Reppert, S.M. & Weaver, D.R. (2002) Coordination of circadian timing in mammals. Nature, 418, 935-941.
32. Salazar-Juárez, A., Aguilar-Roblero, R., Parra, L. & Escobar, C. (2003) Restricted feeding schedules modulate free-running drinking activity in malnourished rats. Biol Rhythms Res., 34, 459-474.
33. Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., McNamara, P., Naik, K.A., FitzGerald, G.A., Kay, S.A. & Hogenesch, J.B. (2004) A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron, 43, 527-537.
34. Schwartz, M.D., Nunez, A.A. & Smale, L. (2004) Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience, 127, 13-23.
35. Shearman, L.P., Zylka, M.J., Weaver, D.R., Kolakowski, L.F. Jr & Reppert, S.M. (1997) Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron, 19, 1261-1269.
36. Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., Moriya, T., Shibata, S., Loros, J.J., Dunlap, J.C. & Okamura, H. (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell, 91, 1043-1053.
37. Slotten, H.A., Pitrosky, B., Krekling, S. & Pevet, P. (2002) Entrainment of circadian activity rhythms in rats to melatonin administered at T cycles different from 24 hours. Neurosignals, 11, 73-80.
38. Stephan, F.K. (2001) Food-entrainable oscillators in mammals. In Takahashi, J.S., Turek, F.W. & Moore, R.Y. (Eds), Circadian Clocks, Vol. 12 Handbook of Behavioral Neurobiology. Kluwer Academic/Plenum Publishers, New York, pp. 223-246.
39. Sun, Z.S., Albrecht, U., Zhuchenko, O., Bailey, J., Eichele, G. & Lee, C.C. (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell, 90, 1003-1011.
40. Tei, H., Okamura, H., Shigeyoshi, Y., Fukuhara, C., Ozawa, R., Hirose, M. & Sakaki, Y. (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature, 389, 512-516.
41. Tournier, B.B., Menet, J.S., Dardente, H., Poirel, V.J., Malan, A., Masson-Pevet, M., Pevet, P. & Vuillez, P. (2003) Photoperiod differentially regulates clock genes' expression in the suprachiasmatic nucleus of Syrian hamster. Neuroscience, 118, 317-322.
42. Wakamatsu, H., Yoshinobu, Y., Aida, R., Moriya, T., Akiyama, M. & Shibata, S. (2001) Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur. J. Neurosci., 13, 1190-1196.
43. Yan, L., Takekida, S., Shigeyoshi, Y. & Okamura, H. (1999) Per1 and Per2 gene expression in the rat suprachiasmatic nucleus: circadian profile and the compartment-specific response to light. Neuroscience, 94, 141-150.
44. Zylka, M.J., Shearman, L.P., Weaver, D.R. & Reppert, S.M. (1998) Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron, 20, 1103-1110.