Daily Rhythm of Spontaneous Immediate-Early Gene Expression in the Rat Suprachiasmatic Nucleus

Abstract

Nocturnal light induces the expression of various immediate-early genes (IEGs) in the suprachiasmatic nucleus (SCN), the primary pacemaker of the circadian system of mammals, and causes phase shifts of behavioral rhythms. In the hamster SCN, some IEGs show both sensitivity to light induction at night and a daily peak of spontaneous expression near dawn in different regions of the nucleus. To investigate whether both patterns of IEG expression are observed in the rat SCN, the authors studied the expression of NGFI-A, junB, c-fos, and fosBnear the time of subjective dawn in rats entrained to a light-dark 12:12 cycle and then maintained in constant total darkness for ~48 h. They found that there were two independent rhythms of expression for junB and c-fos mRNAs in the SCN: (1) a rhythm of photic sensitivity expressed throughout the night and (2) a spontaneous rhythm of expression triggered around dawn and persisting for at least 2 h into the day. By contrast, fosB and NGFI-A transcripts were expressed only after light exposure at night and did not exhibit significant levels of spontaneous expression in the absence of photic input. These observations demonstrate that the circadian clock gates expression of two independent rhythms related to IEG expression in the rat SCN. The rhythm of sensitivity to nocturnal light exposure is expressed more strongly in the ventral SCN and may be related to photic entrainment. The second rhythm is triggered spontaneously in darkness around subjective dawn and is expressed in more dorsal parts of the SCN.

Keywords

suprachiasmatic nucleus circadian rhythm junB c-fos fosB NGFI-A immediate-early gene spontaneous expression transcription regulation

References

Albrecht U , Sun ZS , Eichele G , and Lee CC (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91:1055-1064.

Chiasson BJ , Hong ML , and Robertson HA (1998) Intraamygdala infusion of an end-capped antisense oligodeoxynucleotide to c-fos accelerates amygdala kindling. Mol Brain Res 57:248-256.

Guido ME , Goguen D , de Guido L , Robertson HA , and Rusak B (1999) Circadian and photic regulation of immediate-early gene expression in the hamster supra-chiasmatic nucleus. Neurosci 90:555-571.

Guido ME , Goguen D , Robertson HA , and Rusak B (1996a) Spontaneous and light-evoked expression of JunB-like protein in the hamster suprachiasmatic nucleus near subjective dawn. Neurosci Lett 217:9-12.

Guido ME , Rusak B , and Robertson HA (1996b) Spontaneous circadian and light-induced expression of junBmRNA in the hamster suprachiasmatic nucleus. Brain Res 732:215-222.

Kornhauser JM , Nelson DE , Mayo KE , and Takahashi JS (1990) Photic and circadian regulation of c-fos gene expression in the hamster suprachiasmatic nucleus. Neuron 5:127-134.

Kornhauser JM , Nelson DE , Mayo KE , and Takahashi JS (1992) Regulation of junB messenger RNA and AP-1 activity by light and a circadian clock. Science 255:1581-1584.

Lin JT , Kornhauser JM , Singh NP , Mayo KE , and Takahashi JS (1997) Visual sensitivities of nur77 (NGFI-B) and zif268 (NGFI-A) induction in the suprachiasmatic nucleus are dissociated from c-fos induction and behavioral phaseshifting responses. Mol Brain Res 46:303-310.

Majzoub JA , Robinson BC , and Emanuel RL (1991) Suprachiasmatic nuclear rhythms of vasopressin mRNA in vivo. In Suprachiasmatic Nucleus: The Mind's Clock, DC Klein , RY Moore , and SM Reppert , eds, pp 177-190, Oxford University Press, New York.

10.

Milbrandt J (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238:797-799.

11.

Morgan J and Curran T (1991) Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451.

12.

Peters RV , Aronin N , and Schwartz WJ (1994) Circadian regulation of FosB is different from c-Fos in the rat suprachiasmatic nucleus. Mol Brain Res 27:243-248.

13.

Robertson HA (1992) Immediate-early genes, neuronal plasticity, and memory. Biochem Cell Biol 70:729-737.

14.

Rocha L and Kaufman DL (1998) In vivo administration of c-fos antisense oligonucleotides accelerates amygdala kindling. Neurosci Lett 241:111-114.

15.

Rusak B , McNaughton L , Robertson HA , and Hunt SP (1992) Circadian variation in photic regulation of immediate early gene mRNAs in rat suprachiasmatic nucleus cells. Mol Brain Res 14:124-130.

16.

Rusak B , Robertson HA , Wisden W , and Hunt SP (1990) Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science 248:1237-1240.

17.

Ryder K , Lau LF , and Nathans D (1988) A gene activated by growth factors is related to the oncogene v-jun. Proc Natl Acad Sci USA 85:1487-1491.

18.

Shigeyoshi Y , Taguchi K , Yamamoto S , Takekida S , Yan L , Tei H , Moriya T , Shibata S , Loros JJ , Dunlap JC , and Okamura H (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91:1043-1053.

19.

Shinohara K , Isobe Y , Takeuchi J , and Inouye SIT (1991) Circadian rhythms of somatostatin-immunoreactivity in the suprachiasmatic nucleus of the rat. Neurosci Lett 129:59-62.

20.

Sumová A , Trávnícková Z , Mikkelsen JD , and Illnerov H (1998) Spontaneous rhythm in c-Fos immunoreactivity in the dorsomedial part of the rat suprachiasmatic nucleus. Brain Res 801:254-258.

21.

Sun ZS , Albrecht U , Zhuchenko O , Bailey J , Eichele G , and Lee CC (1997) RIGUI, a putative mammalian ortholog of the Drosophila period gene. Cell 90:1003-1011.

22.

Sutin EL and Kilduff TS (1992) Circadian and light-induced expression of immediate-early gene mRNAs in the rat suprachiasmatic nucleus. Mol Brain Res 15:281-290.

23.

Takeuchi J , Shannon W , Aronin N , and Schwartz WJ (1993) Compositional changes of AP-1 DNA-binding proteins are regulated by light in a mammalian circadian clock. Neuron 11:825-836.

24.

Tanaka M , Amaya F , Tamada Y , Okamura H , Hisa Y , and Ibata Y (1997) Induction of NGFI-A gene expression in the rat suprachiasmatic nucleus by photic stimulation. Brain Res 756:305-310.

25.

Tei H , Okamura H , Shigeyoshi Y , Fukuhara C , Ozawa R , Hirose M , and Sakaki Y (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 389:512-516.

26.

Van Beveren C , van Straatan F , Curran T , Müller R , and Verma I (1983) Analysis of FBJ-MuSV Provirus and c-fos(Mouse) gene reveals that viral and cellular fos gene products have different carboxy termini. Cell 32:1241-1255.

27.

van den Pol A (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.

28.

Wollnik F , Brysh W , Uhlmann E , Gillardon F , Bravo R , Zimmermann M , Schlingensiepen KH , and Herdegen T (1995) Block of c-Fos and JunB expression by antisense oligonucleotides inhibits light-induced phase shifts of the mammalian circadian clock. Eur J Neurosci 7:388-393.

29.

Zerial M , Toschi L , Ryseck R-P , Schuermann M , Muller R , and Bravo R (1989) The product of a novel growth factor activated gene, fosB, interacts with Jun proteins enhancing their DNA binding activity. EMBO J 8:805-813.