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E-Box Function in a Period Gene Repressed by Light

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E-Box Function in a Period Gene Repressed by Light E-box function in a period gene repressed by light Daniela Vallone*, Srinivas Babu Gondi*, David Whitmore†, and Nicholas S. Foulkes*‡ *Max-Planck-Institut fu¨r Entwicklungsbiologie, Spemannstrasse 35-39, Tu¨bingen, D-72076 Germany; and †Centre for Cell and Molecular Dynamics, Department of Anatomy and Developmental Biology, University College London, 21 University Street, London WC1E 6JJ, England Edited by Jeffrey C. Hall, Brandeis University, Waltham, MA, and approved January 14, 2004 (received for review September 11, 2003) In most organisms, light plays a key role in the synchronization of the forced changes in running wheel activity (17). The precise contri- circadian timing system with the environmental day–night cycle. bution of these genes to clock entrainment by light remains unclear Light pulses that phase-shift the circadian clock also induce the (18–20). expression of period (per) genes in vertebrates. Here, we report the The E-box (CACGTG) is a key component of the circadian clock. cloning of a zebrafish per gene, zfper4, which is remarkable in being Depending on the time of day, it mediates either transcriptional repressed by light. We have developed an in vivo luciferase reporter activation or repression (10). However, this element is also the assay for this gene in cells that contain a light-entrainable clock. binding site for a multitude of other basic helix–loop–helix tran- High-definition bioluminescence traces have enabled us to accurately scription factors (21). Only a subset of E-boxes, termed circadian, measure phase-shifting of the clock by light. We have also exploited seem to represent specific binding sites for Clock–BMAL het- this model to study how four E-box elements in the zfper4 promoter erodimers (21–24). Additional sequences flanking the core hex- regulate expression. Mutagenesis reveals that the integrity of these amer as well as the presence of multiple, randomly spaced E-boxes four E-boxes is crucial for maintaining low basal expression together in a promoter region have been reported to favor circadian-clock with robust rhythmicity and repression by light. Importantly, in the regulation (25, 26). context of a minimal heterologous promoter, the E-box elements also The proven usefulness of the zebrafish for large-scale genetic direct a robust circadian rhythm of expression that is significantly screens makes it an attractive model to study the circadian clock (27, phase-advanced compared with the original zfper4 promoter and 28). Zebrafish peripheral clocks are directly light entrainable, lacks the light-repression property. Thus, these results reveal flexibil- implying the widespread expression of a circadian photopigment in ity in the phase and light responsiveness of E-box-directed rhythmic this vertebrate (29). Zebrafish embryo-derived cell lines express a expression, depending on the promoter context. light-entrainable clock (29, 30), making them a potentially powerful in vitro model system. Sustained circadian rhythms of clock gene he use of an endogenous pacemaker or clock to anticipate expression can be established simply by exposing cultures to LD Tand thereby respond appropriately to day–night changes in cycles. This situation contrasts with mammalian cell lines such as the environment has been a highly conserved strategy through- rat-1 fibroblasts, in which only rapidly dampening rhythms enduring out evolution (1). This clock is entrained daily by environmental four or five cycles can be induced by transient treatment with timing signals, so-called zeitgebers such as temperature and light, various signals (31, 32). Three zebrafish per genes have been and so remains synchronized with the light–dark (LD) cycle. described to date, homologs of mper1, 2, and 3 (30, 33–35). Whereas Characteristically, under constant darkness (DD) or constant the clock regulates expression of zfper1 and 3, light activates zfper2 light (LL), the period of the clock rhythm deviates slightly from (30, 36). A blue light photoreceptor coupled to the mitogen- 24 h, and hence, it is termed circadian. This defining property is activated protein kinase pathway has been implicated in mediating thought to ensure optimal entrainment by zeitgebers (2). In light-induced expression of zfper2 (36). vertebrates, the circadian clock was originally thought to reside Here, we report the cloning of a zebrafish per gene, zfper4. Its in a small number of specialized pacemakers: the suprachias- expression in larvae and a zebrafish cell line reveals this to be an matic nucleus, the retina, and in lower vertebrates, the pineal example of a per gene that is repressed by light. By using an in vivo gland (3, 4). However, rhythmic clock gene expression was luciferase assay, we have visualized its expression in the PAC-2 cells. encountered subsequently in vivo in most cell types (5, 6) and We show that the integrity of four E-box elements within the zfper4 shown to persist in vitro (7, 8). Thus, the circadian clock seems promoter is essential for a low basal expression level, robust to be a fundamental property of most cells. rhythmic expression, and repression by light. Interestingly, the Many clock genes encode transcriptional regulators, which are phase of the rhythm directed by the E-boxes and its acute response components of autoregulatory feedback loops (9, 10). In verte- to light seems to be a function of the promoter context. brates, the transcription factors Clock and brain and muscle arnt- like protein (BMAL) bind as heterodimers to E-box enhancers and Materials and Methods activate the expression of other clock genes that encode transcrip- Cloning of the zfper4 Gene. The following oligonucleotides based on tional repressors: the Period (Per) and Cryptochrome (Cry) pro- the Xenopus per1 cDNA (37) were used to prime long-distance PCR teins. These repressors complex with Clock–BMAL and interfere (XL PCR kit, Perkin–Elmer) with PAC-2 DNA (38): AF250547 with transcriptional activation, thereby reducing expression of their and BE679697, 5Ј-AGTGGCTGCAGCAGTGAACAGTCT- own genes and closing the feedback loop (9, 10). GCC-3Ј (sense); and 5Ј-CCAAAGTATTTGCTGGTGTTGCT- After the original characterization of the period locus in Dro- GCTC-3Ј (antisense). The products were analyzed by Southern sophila, there was a long delay before the first vertebrate per gene blotting using an mper1 PAS domain probe (12), purified by using homolog was cloned (11, 12). Subsequently, multiple per genes were the QIAquick gel extraction kit (Qiagen, Valencia, CA), and then identified, suggesting either redundancy or specialization of func- cloned into pGemT-easy (Promega) for sequencing. RACE PCR tion of the various family members (6). Three per genes have been identified in the mouse that play distinct roles in the circadian clock mechanism (6, 13). Whereas mper1 and mper2 seem to be essential, This paper was submitted directly (Track II) to the PNAS office. mper3 is dispensable for circadian rhythmicity (14). Both mper1 and Abbreviations: LD, light–dark; DD, constant darkness; LL, constant light; BMAL brain and mper2 are expressed with a circadian rhythm and are rapidly muscle arnt-like protein. induced in the suprachiasmatic nucleus by light pulses delivered Data deposition: The sequence reported in this paper has been deposited in the GenBank during the subjective night but not during the subjective day (6, 15, database (accession no. AY359820). 16). Also, repression of mper1 expression in the suprachiasmatic ‡To whom correspondence should be addressed. E-mail: [email protected]. nucleus has been observed during phase-shifting of the clock by © 2004 by The National Academy of Sciences of the USA 4106–4111 ͉ PNAS ͉ March 23, 2004 ͉ vol. 101 ͉ no. 12 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0305436101 Downloaded by guest on September 28, 2021 (Marathon cDNA amplification kit, Clontech) and long-distance internal control. The quoted fold-activation and repression values PCR were used to clone the full-length zfper4 cDNA and genomic are the mean of at least three independent experiments. region. Phase–Response Curve Analysis. zfper4 promoter-luciferase reporter Promoter Reporter Constructs. The zfper4 promoter was amplified by cells were plated in 10 plates in medium supplemented with using GenomeWalker PCR (Clontech) and subcloned into luciferin. All plates were exposed for 3 days to an LD cycle; on the pGL3Basic (Promega). Two canonical and two noncanonical E- fourth day, they were individually sealed in light-proof boxes. After boxes were mutated to CTCGAG by site-directed mutagenesis 3 complete days in DD, individual plates were light pulsed for 1 or (Stratagene). Oligonucleotides consisting of four copies of the 4 h, at 3- or 4-h intervals, respectively, by using a tungsten light sequence; 5Ј-GAAGCACGTGTACTCG-3Ј (E-box, position Ϫ7) source (20 ␮W͞cm2). One control plate remained in DD. After the was cloned into pLucMCS (Stratagene) to generate 4ϫ E-box(Ϫ7). final light pulse, all plates were counted for 3 days in DD. Stable phase-shifts for each light-treated plate relative to the DD control Oligonucleotide Synthesis and Sequence Analysis. All oligonucleo- on the third day were then calculated. The time of onset of each light tides were synthesized by MWG Biotec (Ebersberg, Germany). pulse was expressed in circadian time (CT), where CT0 is defined Sequencing was performed by the MPI genome analysis service. as the beginning of the subjective day and CT12, the beginning of Database searches and alignments were made by using BLAST. the subjective night. The duration of one free running period is 24 Consensus transcription factor binding sites were identified by CT h. In terms of the zfper4 luciferase rhythm, CT0 is defined as 3.2 comparison with the Transfac transcription factor database. actual hours before each peak. Phase shifts were also expressed as circadian hours by multiplying actual hour times by 24͞␶ (40). Establishment of Stable Cell Lines. PAC-2 cells (29, 38) were culti- Results vated as described (29). Cells were transfected with linearized plasmids; the luciferase reporter and a neomycin resistance plasmid Expression of the zfper4 Gene.
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