Rhythmicity of the rat suprachiasmatic nucleus (SCN), a site of the circadian pacemaker, is affected by daylength; that is, by the photoperiod. Whereas various markers of rhythmicity have been followed, so far there have been no studies on the effect of the photoperiod on the expression of the clock genes in the rat SCN. To fill the gap and to better understand the photoperiodic modulation of the SCN state, rats were maintained either under a long photoperiod with 16 h of light and 8 h of darkness per day (LD16:8) or under a short LD8:16 photoperiod, and daily profiles of Per1, Cry1, Bmal1 and Clock mRNA in darkness were assessed by in situ hybridization method. The photoperiod affected phase, waveform, and amplitude of the rhythmic gene expression as well as phase relationship between their profiles. Under the long period, the interval of elevated Per1 mRNA lasted for a longer and that of elevated Bmal1 mRNA for a shorter time than under the short photoperiod. Under both photoperiods, the morning and the daytime Per1 and Cry1 mRNA rise as well as the morning Bmal1 mRNA decline were closely linked to the morning light onset. Amplitude of Per1, Cry1, and Bmal1 mRNA rhythms was larger under the short than under the long photoperiod. Also, under the short photoperiod, the daily Clock mRNA profile exhibited a significant rhythm. Altogether, the data indicate that the whole complex molecular clockwork in the rat SCN is photoperiod dependent and hence may differ according to the season of the year.
References
1.
Bae K, Jin X, Maywood ES, Hastings MH, Reppert SM, and Weaver DR (2001) Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron30: 525-536.
2.
Cagampang FR, Yang J, Nakayama J, Fukuhara C, and Ynouye ST (1994) Circadian variation of arginine-vasopressin messenger RNA in the rat suprachiasmatic nucleus. Mol Brain Res24: 179-184.
3.
Daan S, Albrecht U, van der Horst GTJ, Illnerová H, Roenneberg T, Wehr TA, and Schwartz WJ (2001) Assembling a clock for all seasons: Are there M and E oscillators in the genes? J Biol Rhythms16: 105-116.
4.
Elliot JA and Tamarkin L (1994) Complex circadian regulation of pineal melatonin and wheel-running in Syrian hamsters. J Comp Physiol [A]174: 469-484.
5.
Field MD, Maywood ES, O’Brien JA, Weaver DR, Reppert SM, and Hastings MH (2000) Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron25: 437-447.
6.
Goldman BD and Darrow JM (1983) The pineal gland and mammalian photoperiodism. Neuroendocrinology37: 368-396.
7.
Guido ME, deGuido JB, Goguen D, Robertson HA, and Rusak B (1999) Daily rhythm of spontaneous immediate-early gene expression in the rat suprachiasmatic nucleus. J Biol Rhythms14: 275-280.
8.
Harrington ME and Rusak B (1986) Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. J Biol Rhythms1: 309-325.
9.
Hastings M (2001) Modeling the molecular calendar. J Biol Rhythms16: 117-123.
10.
Illnerová H (1988) Entrainment of mammalian circadian rhythms in melatonin production by light. Pineal Res Rev6: 173-217.
11.
Illnerová H (1991) The suprachiasmatic nucleus and the rhythmic pineal melatonin production. In Suprachiasmatic Nucleus: The Mind’s Clock, DC Klein, RY Moore, and SM Reppert, eds, pp 197-216, Oxford University Press, New York.
12.
Illnerová H, Sumová A, Trávníčková Z, Jáč M, and Jelínková D (2000) Hormones, subjective night and season of the year. Physiol Res49: 1-10.
13.
Illnerová H and Vaněček J (1980) Pineal rhythm in N-acetyltransferase activity in rats under different artificial photoperiods and in natural daylight in the course of a year. Neuroendocrinology31: 321-326.
14.
Jáč M, Kiss A, Sumová A, Illnerová H, and Ježová D (2000a) Daily profiles of arginine vasopressin mRNA in the suprachiasmatic, supraopticus and paraventricular nuclei of the rat hypothalamus under various photoperiods. Brain Res887: 472-476.
15.
Jáč M, Sumová A, and Illnerová H (2000b) c-Fos rhythm in subdivisions of the rat suprachiasmatic nucleus under artificial and natural photoperiods. Am J Physiol Regul Integr Comp Physiol279: R2270-R2276.
16.
Jin X, Shearman LP, Weaver DR, Zylka MJ, deVries GJ, and Reppert SM (1999) A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell96: 57-68.
17.
King DP and Takahashi JS (2000) Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci23: 713-742.
18.
Klein DC and Moore RY (1979) Pineal N-acetyltransferase and hydroxyindole-O-methyltransferase: Control by the retinohypothalamic tract and the suprachiasmatic nucleus. Brain Res174: 245-262.
19.
Kornhauser JM, Mayo KE, and Takahashi JS (1993) Immediate-early gene expression in a mammalian circadian pacemaker: The suprachiasmatic nucleus. In Molecular Genetics of Biochemical Rhythms, MW Young, ed, pp 271-307, Dekker, New York.
20.
Leak RK, Card JP, and Moore RY (1999) Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport. Brain Res8: 23-32.
21.
Lincoln G, Messager S, Andersson H, and Hazlerigg D (2002) Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: Evidence for an internal coincidence timer. Proc Natl Acad Sci USA99: 13890-13895.
22.
Maywood ES, Mrosovsky N, Field MD, and Hastings MH (1999) Rapid down regulation of mammalian period genes during behavioral resetting of the circadian clock. Proc Natl Acad Sci USA96: 15211-15216.
23.
Messager S, Hazlerigg DG, Mercer JG, and Morgan PJ (2000) Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur J Neurosci12: 2865-2870.
24.
Messager S, Ross AW, Barret P, and Morgan PJ (1999) Decoding photoperiodic time through Per1 and ICER gene amplitude. Proc Natl Acad Sci USA96: 9938-9943.
25.
Miyazaki K, Mesaki M, and Ishida A (2001) Nuclear entry mechanism of rat PER2 (rPER2): Role of rPER2 in nuclear localization of CRY protein. Mol Cell Biol21: 6651-6659.
26.
Moore RY (1996) Entrainment pathways and functional organization of the circadian timing system. In Hypothalamic Integration of Circadian Rhythms, RM Buijs, A Kalsbeek, HJ Romijn, CM Pennartz, and A Mirmiram, eds, pp 101-117, Elsevier, Amsterdam.
27.
Mrugala M, Zlomanczuk P, Jagota A, and Schwartz WJ (2000) Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am J Physiol Regul Integr Comp Physiol278: R987-R994.
28.
Nuesslein-Hildesheim B, O’Brien JA, Ebling FJ, Maywood ES, and Hastings MH (2000) The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the Siberian hamster encodes both daily and seasonal time. Eur J Neurosci12: 2856-2864.
29.
Pittendrigh CL (1981) Circadian systems: Entrainment. In Biological Rhythms: Handbook of Behavioral Neurology, Vol 4, J Aschoff, ed, pp 95-124, Plenum, New York.
30.
Preitner A, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, and Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell110: 251-260.
31.
Reppert SM and Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol63: 647-676.
32.
Schwartz WJ, Aronin N, Takeuchi J, Bennet MR, and Peters RJ (1995) Towards a molecular biology of the suprachiasmatic nucleus: Photic and temporal regulation of c-fos gene expression. Semin Neurol7: 53-60.
33.
Schwartz WJ, Caprio A Jr, de la Iglesia HO, Baler R, Klein DC, Nakabeppu Y, and Aronin N (2000) Differential regulation of fos family genes in the ventrolateral and dorsomedial subdivisions of the rat suprachiasmatic nucleus. Neuroscience98: 535-547.
34.
Schwartz WJ, de la Iglesia HO, Zlomanczuk P, and Illnerová H (2001) Encoding Le Quattro Stagioni within the mammalian brain: Photoperiodic orchestration through the suprachiasmatic nucleus. J Biol Rhythms16: 302-311.
35.
Shearman LP, Jin X, Lee C, Reppert SM, and Weaver DR (2000) Targeted disruption of the mPer3 gene: Subtle effect on circadian clock function. Mol Cell Biol20: 6269-6275.
36.
Steinlechner S, Jacobmeier B, Scherbarth F, Dernbach H, Kruse F, and Albrecht U (2002) Robust circadian rhythmicity of Per1 and Per2 mutant mice in constant light and dynamics of Per1 and Per2 gene expression under long and short photoperiods. J Biol Rhythms17: 202-209.
37.
Sumová A, Sládek M, Jáč M, and Illnerová H (2002) The circadian rhythm of Per1 gene product in the rat suprachiasmatic nucleus and its modulation by seasonal changes in daylength. Brain Res947: 260-270.
38.
Sumová A, Trávníčková Z, and Illnerová H (1995a) Memory on long but not on short days is stored in the rat suprachiasmatic nucleus. Neurosci Lett200: 191-194.
39.
Sumová A, Trávníčková Z, and Illnerová H (2000) Spontaneous c-Fos rhythm in the rat suprachiasmatic nucleus: Location and effect of photoperiod. Am J Physiol Regul Integr Comp Physiol279: R2262-R2269.
40.
Sumová A, Trávníčková Z, Mikkelsen JD, and Illnerová H (1998) Spontaneous rhythm in c-Fos immunoreactivity in the dorsomedial part of the rat suprachiasmatic nucleus. Brain Res801: 254-258.
41.
Sumová A, Trávníčková Z, Peters R, Schwartz WJ, and Illnerová H (1995b) The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci USA92: 7754-7758.
42.
Tamaru T, Isojima Y, Yamada T, Okada M, Nagai K, and Takamatsu K (2000) Light and glutamate-induced degradation of the circadian oscillating protein BMAL1 during the mammalian clock resetting. J Neurosci20: 7525-7530.
43.
Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, et al. (2002) A transcription factor response element for gene expression during circadian night. Nature418: 534-539.
44.
van den Pol AN (1991) The suprachiasmatic nucleus: Morphological and cytochemical substrates for cellular interaction. In Suprachiasmatic Nucleus: The Mind’s Clock, DC Klein, RY Moore, and SM Reppert, eds, pp 17-50, Oxford University Press, New York.
45.
Yagita K, Tamanini F, Yasuda M, Hoeijmakers JHJ, van der Horst GTJ, and Okamura H (2002) Nucleocytoplasmic shuttling and mCRY-dependent inhibition of ubiquitylation of mPER2 clock protein. EMBO J21: 1301-1314.
46.
Yagita K, Yamaguchi S, Tamanini F, van der Horst GTJ, Hoeijmakers JHJ, Yasui A, Loros L, Dunlap JC, and Okamura H (2000) Dimerization and nuclear entry of mPER proteins in mammalian cells. Genes Develop14: 1353-1363.
47.
Yu W, Nomura M, and Ikeda M (2002) Interacting feedback loops within the mammalian clock: BMAL1 is negatively autoregulated and upregulated by CRY1, CRY2, and PER2. Biochem Biophys Res Commun290: 933-941.
48.
Zheng B, Albrecht U, Kaasil K, Sage M, Lu W, Vaishnav S, Li Q, Sun ZS, Eichele G, Bradley A, et al. (2001) Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell105: 683-694.
