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Mechanism of Circadian Clock. the 2017 Nobel Prize in Physiology Or Medicine

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Mechanism of Circadian Clock. the 2017 Nobel Prize in Physiology Or Medicine Tom 67 2018 Numer 2 (319) Strony 245–249 JADWIGA M. GIEBULTOWICZ Oregon State University Department of Integrative Biology 3029 Cordley Hall Corvallis, OR 97331 USA E-mail: [email protected] MECHANISM OF CIRCADIAN CLOCK. THE 2017 NOBEL PRIZE IN PHYSIOLOGY OR MEDICINE Most animals lead rhythmic lives; some ferent species suggested that the clock may are active at night and sleep during the have genetic basis, because the period of day, while others are diurnal, being active free-running rhythms could be inherited, or during daytime. Although these rhythms modulated by long term selection. Yet, the have a period of 24 hours matching the so- mechanism of circadian clocks remained a lar day, they are not merely a response to total mystery until researchers working with a daylight or darkness at night. When ani- fruit flies, Drosophila melanogaster, decided mals are placed in constant conditions such to test experimentally whether genes are in- as constant darkness and constant temper- volved in the clock function. Fruit flies have ature, they do not lose a sense of time but been used as a genetic model for over a maintain rhythmicity of rest and activity. hundred years; in the early 20th century, However, in these conditions, the period be- US biologist Thomas Morgan used fruit flies tween two sequential activity onsets is not to confirm that genes are located on chro- exactly 24 hours, but rather it is about or mosomes like beads on a string, and estab- “circa” 24 hours; therefore, these cycles are lished genetics as a modern science. Flies called circadian rhythms. Even humans iso- have a high reproduction rate, short life cy- lated from a solar day and left in artificial cle of 10 days from egg to adult, and there light to schedule their own activities, main- are well-established methods to induce mu- tain a clear circadian rhythm of sleep and tations and map them on fly chromosomes. wakefulness. These types of experiments Working at the California Institute of demonstrate that organisms have evolved Technology (CalTech), Dr. Seymour Ben- their own internal sense of time, which is zer and his graduate student Ron Konop- synchronized daily to a 24h solar cycle but ka decided to use rhythm of emergence of in constant conditions displays its endog- adult flies from their pupal cases to probe enous, free-running nature. The internal the mystery of the clock. Individual adult sense of time allows anticipation of cyclical flies tend to emerge in the morning while life events. For example, before we wake up, no emergence takes place in the afternoon, our internal clock orchestrates an increase and a free-running rhythm of adult emer- in blood pressure and in the levels of hor- gence persists in constant darkness. The mone cortisol to prepare us for activities of experimental approach was to mutate hun- the day. dreds of flies in hope of finding a few that The question of how animals and hu- would emerge at the “wrong” time. Indeed, mans can measure time has intrigued sci- the authors of this study isolated several of entists for many decades. Chronobiogists such flies and by analyzing their progeny named the internal mechanism the “circa- they discovered that a single genomic lo- dian clock” and depicted it as a black box cus, which they named period (per) carried when drawing models. Experiments in dif- three different mutations (KONOPKA and BEN- Key words: biological clock, circadian rhythms, clock genes, Drosophila melanogaster, Nobel Prize 246 JADWIGA M. GIEBULTOWICZ ZER 1971). One mutant completely lost the emergence rhythm (per0), another mutation shortened the free-running rhythm from circa 24h to 19h (pershort), and the third mutation produced long-period rhythms of 29h (perlong) of adult emergence. Excitingly, the same mutations caused corresponding changes in the period of the free-running rhythm of locomotor activity in individual flies, indicating that the period gene is part of the clock controlling different behavioral rhythms. This 1971 discovery of the gene period was the first milestone on the way to un- derstanding biological clocks. However, the sequence and function of period remained unknown until the mid-80s, when three Americans, Drs. Jeffrey Hall and Michael Rosbash at Brandeis University and Mi- chael Young at Rockefeller University, used newly developed genetic and molecular tools to sequence period DNA. The Brandeis and Rockefeller teams independently demonstrat- ed that the introduction of period genomic fragments into an arrhythmic per01 mutant caused rescue of both adult emergence rhythm and locomotor activity rhythm (BAR- GIELLO and YOUNG 1984, REDDY et al. 1984). Further studies in the labs of J. Hall and M. Rosbash showed that PER protein (SI- Fig. 1. Schematic depiction of the negative feed- WICKI et al. 1988) and per mRNA (HARDIN back loop that forms the core mechanism of the et al. 1990) undergo daily oscillations and Drosophila clock. suggested that clock may consist of a nega- tive feedback loop with the PER protein act- At night (upper panel) the CLK/CYC heterodimers bind ing as a repressor of transcription (HARDIN to E-box sequences in per and tim promoters and ac- et al. 1990). Meanwhile, another mutant tivate transcription of these genes. Resulting PER and that abolished circadian rhythms in flies TIM proteins form heterodimers, enter the nucleus and bind to CLK/CYC repressing further transcription of per was uncovered in the lab of M. Young (SE- and tim. Morning light activates the CRY protein (low- HGAL et al. 1994). This second clock gene er panel) which binds to TIM causing its degradation. was named timeless (tim) and the TIM pro- PER, which is stabilized by TIM, also degrades, ending tein turned out to be a partner of PER, the repressive phase of the clock and allowing posi- necessary for its stability and nuclear entry tive arm of the clock to restart. Many clock-controlled (GEKAKIS et al. 1995, VOsshALL et al. 1994) genes (CCGs) also contain E-boxes in their promoters Although it was evident that PER and and their transcription is directly stimulated by CLK/ TIM proteins somehow affected transcrip- CYC. Some of these CCGs encode transcription factors, tion of their own genes, the mechanism was which indirectly generate rhythmic transcription of ad- not clear owing to the lack of DNA-binding ditional CCGs (modified from GIEBULTOWICZ 2017). domains in both proteins. Fortunately, a search for more arrhythmic mutants in the feedback loop is at the core of the circadian labs of J. Hall and M. Rosbash revealed clock in both flies and mammals. A model two genes Clock (Clk) and cycle (cyc) en- of the core feedback loop in Drosophila was coding transcription factors (ALLADA et al. reviewed recently (GIEBULTOWICZ 2017) and 1998, RUTILA et al. 1998) that activate per is shown in Fig. 1. Two transcription fac- and tim mRNA transcription. Interestingly, tors encoded by the genes Clock (Clk) and the Clock gene was first identified as part of cycle (cyc) act as the positive clock factors, the mammalian timing mechanism (VITATER- whereby CLK and CYC proteins form com- NA et al. 1994), and communication between plexes, which bind to the E-box sequenc- fly and mouse researchers greatly facilitated es in the promoters of per and tim genes, the progress in the understanding of the stimulating their transcription in the early circadian clock mechanism. night. After translation, PER and TIM pro- By the turn of the century, it was clear teins act as the negative limb of the clock that the transcription-translation negative when they accumulate in the cell nuclei Mechanism of circadian clock 247 Fig. 2. The poster depicting Nobel Prize winners, from left to right: Jeffrey C. Hall, Michael Rosbash and Michael W. Young. Copyright © The Nobel Assembly at Karolinska Institutet, source, https:// www.nobelprize.org/. late at night and repress CLK-CYC activity. Michael Rosbash and Michael W. Young, This results in the suppression of per and all three of them doing basic research in tim transcription until the repressive PER Drosophila melanogaster. It was not the first and TIM are degraded. Degradation of TIM time that the tiny fruit fly was “honored” in is initiated by light via the photoreceptive this way. At least five other groups have re- CRY protein encoded by the cryptochrome ceived Nobel Prize for their work using fruit (cry) gene characterized in Drosophila by J. flies to decipher the secrets of human phys- Hall and M. Rosbash (EMERY et al. 1998, iology and disease. Sequencing of human STANEWsky et al. 1998). Upon activation by and Drosophila genomes revealed that about light, CRY binds to TIM protein leading to 75% of known human disease genes have its degradation. Because TIM stabilizes PER, a functional match in fruit flies, including the latter is also degraded within few hours genes involved in Down’s syndrome, Alzhei- of lights-on. Mammalian clocks operate by mer’s disease, autism, diabetes, cancer and the same mechanisms and contain mostly others. homologous genes as Drosophila clocks. A Based on early observations of behavio- major difference between fly and mamma- ral rhythms in sleep/activity, feeding, and lian clocks is the use of CRY, rather than cognitive functions, it was assumed that TIM, as the PER binding partner. Mamma- the clock would reside in specialized neu- lian CRY lost light sensitivity and gained a rons. Indeed, the circadian clocks regulating function as the circadian repressor. behavioral functions are located in specific The research that led to the understand- brain neurons of mammals and insects; ing of the circadian clock mechanism earned this was investigated using perturbation of their discoverers the 2017 Nobel Prize locomotor activity rhythms as a readout of in Physiology or Medicine.
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