Light-pulse phase response curves for the locomotor activity rhythm in Period mutants of Drosophila melanogaster

Saunders, D. S.; Gillanders, S. W.; Lewis, R.D.

doi:10.1016/0022-1910(94)90134-1

Cited by 74 publications

(55 citation statements)

References 25 publications

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“…2) have shifted to their steady-state phases. These results are similar to previous results in which a change in the same LD cycle (38) or a pulse of light (3,32) results in a rapid resetting of behavioral activity. Thus, phase shifts of the negative feedback loop due to prolonged light or premature dark are translated into behavioral phase shifts along a similar time course.…”

Section: Discussionsupporting

confidence: 91%

per mRNA Cycling Is Locked to Lights-Off under Photoperiodic Conditions That Support Circadian Feedback Loop Function

Qiu

Hardin

1996

Molecular and Cellular Biology

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Circadian fluctuations in per mRNA and protein are central to the operation of a negative feedback loop that is necessary for setting the free-running period and for entraining the circadian oscillator to light-dark cycles. In this study, per mRNA cycling and locomotor activity rhythms were measured under different light and dark cycling regimes to determine how photoperiods affect the molecular feedback loop and circadian behavior, respectively. These experiments reveal that per mRNA peaks in abundance 4 h after lights-off in photoperiods of <16 h, that phase shifts in per mRNA cycling and behavioral rhythmicity occur rapidly after flies are transferred from one photoperiod to another, and that photoperiods longer than 20 h abolish locomotor activity rhythms and leave per mRNA at a median constitutive level. These results indicate that the per feedback loop uses lights-off as a phase reference point and suggest (along with previous findings for per 01 and tim 01 ) that per mRNA cycling is not regulated via simple negative feedback from the per protein.Circadian rhythms in biochemical, physiological, and behavioral phenomena are a fundamental adaptation of both prokaryotic and eukaryotic organisms to environmental changes that occur over a 24-h period. These rhythms are driven by an endogenous clock that continues to operate under constant environmental conditions. The timekeeping component of the clock, or pacemaker, maintains a periodicity that can be hours longer or shorter than 24 h, and it is synchronized to local time by such environmental signals as light and dark. A stable phase relationship between the pacemaker and its Zeitgeber is clearly a prerequisite if preprogrammed biological changes are to be appropriately timed to daily environmental changes. Physiological and behavioral experiments have been used to determine how the clock adjusts its phase to circadian cycles composed of different proportions of light and dark. During these different photoperiodic conditions, the phase of the circadian pacemaker (and its physiological and behavioral output) is altered so that a stable phase relationship is maintained (26). Because of the lack of measurable pacemaker components, however, these physiological studies could not address the molecular mechanism by which the clock adjusts its phase to accommodate different environmental light-dark (LD) cycles.Genetic screens for rhythm mutants have been used to identify components of the circadian pacemaker. Mutations in the per gene from Drosophila melanogaster can shorten (per S and per) circadian rhythms of locomotor activity and eclosion during constant dark (DD) conditions (16,17) and alter the phase of locomotor activity and eclosion rhythms during LD cycling conditions (3,10,11,17,30). These behavioral effects of the per mutants are paralleled at the molecular level by circadian fluctuations in the abundance of per mRNA and per protein (PER) (12, 41). These fluctuations in per mRNA and protein levels compose a negative feedback loop in which per mRNA serves ...

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Section: Discussionsupporting

confidence: 91%

per mRNA Cycling Is Locked to Lights-Off under Photoperiodic Conditions That Support Circadian Feedback Loop Function

Qiu

Hardin

1996

Molecular and Cellular Biology

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“…Comas et al (2006) systematically monitored PRCs for single light pulses of different duration (1,3,4,6,9,12, and 18 hours) in mice. As expected, they found that longer light pulses caused a higher PRC amplitude, an effect that was also observed in other species including humans and flies (Gander and Lewis, 1983;Czeisler et al, 1989;Saunders et al, 1994). Here, we found that control flies increased phase delays to 11 hours (and phase advances to ~6 hours) when light pulse duration was extended to 6 hours, making understandable why fruit flies can entrain immediately to an 8-hour phase delay of the 12:12 LD cycle (Fig.…”

Section: Discussionsupporting

confidence: 88%

“…This indicates that the 2 methods to monitor a PRC yield very similar results in D. melanogaster. The magnitudes of phase shifts were also very similar to the other PRCs recorded for wild-type flies (Saunders et al, 1994;Emery et al, 1998;Rutila et al, 1998;Stanewsky et al, 1998;Suri et al, 1998): approximately 4 hours for phase delays and 1 to 3 hours for phase advances. This indicates that magnitudes depend little on the used light intensity ranging from 300 to 2000 lux and pulse duration from 10 minutes to 1 hour.…”

Section: Discussionsupporting

confidence: 77%

Phase-Shifting the Fruit Fly Clock without Cryptochrome

et al. 2012

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The blue light photopigment cryptochrome (CRY) is thought to be the main circadian photoreceptor of Drosophila melanogaster. Nevertheless, entrainment to light-dark cycles is possible without functional CRY. Here, we monitored phase response curves of cry 01 mutants and control flies to 1-hour 1000-lux light pulses. We found that cry 01 mutants phase-shift their activity rhythm in the subjective early morning and late evening, although with reduced magnitude. This phase-shifting capability is sufficient for the slowed entrainment of the mutants, indicating that the eyes contribute to the clock's light sensitivity around dawn and dusk. With longer light pulses (3 hours and 6 hours), wild-type flies show greatly enhanced magnitude of phase shift, but CRY-less flies seem impaired in the ability to integrate duration of the light pulse in a wild-type manner: Only 6-hour light pulses at circadian time 21 significantly increased the magnitude of phase advances in cry 01 mutants. At circadian time 15, the mutants exhibited phase advances instead of the expected delays. These complex results are discussed.

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“…For example, the light-induced degradation of TIM in the early or late night either delays or advances, respectively, the PER-TIM temporal program (21,25,32,53). These findings can explain the main features of the light PRC for Drosophila behavioral rhythms, with its characteristic nonresponsive zone in the subjective day, phase delays in the early night, and phase advances in the late night (6,26,32,34,42).…”

mentioning

confidence: 98%

Differential Effects of Light and Heat on the Drosophila Circadian Clock Proteins PER and TIM

Sidote

Majercak

Parikh³

et al. 1998

Molecular and Cellular Biology

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Circadian (Х24-h) rhythms are governed by endogenous biochemical oscillators (clocks) that in a wide variety of organisms can be phase shifted (i.e., delayed or advanced) by brief exposure to light and changes in temperature. However, how changes in temperature reset circadian timekeeping mechanisms is not known. To begin to address this issue, we measured the effects of short-duration heat pulses on the protein and mRNA products from the Drosophila circadian clock genes period (per) and timeless (tim). Heat pulses at all times in a daily cycle elicited dramatic and rapid decreases in the levels of PER and TIM proteins. PER is sensitive to heat but not light, indicating that individual clock components can markedly differ in sensitivity to environmental stimuli. A similar resetting mechanism involving delays in the per-tim transcriptional-translational feedback loop likely underlies the observation that when heat and light signals are administered in the early night, they both evoke phase delays in behavioral rhythms. However, whereas previous studies showed that the light-induced degradation of TIM in the late night is accompanied by stable phase advances in the temporal regulation of the PER and TIM biochemical rhythms, the heat-induced degradation of PER and TIM at these times in a daily cycle results in little, if any, long-term perturbation in the cycles of these clock proteins. Rather, the initial heat-induced degradation of PER and TIM in the late night is followed by a transient and rapid increase in the speed of the PER-TIM temporal program. The net effect of these heat-induced changes results in an oscillatory mechanism with a steady-state phase similar to that of the unperturbed control situation. These findings can account for the lack of apparent steady-state shifts in Drosophila behavioral rhythms by heat pulses applied in the late night and strongly suggest that stimulus-induced changes in the speed of circadian clocks can contribute to phase-shifting responses.Circadian (Х24-h) rhythms are governed by endogenous biochemical oscillators, or clocks (reviewed in references 18 and 46). Although these rhythms persist under constant environmental conditions, they can be entrained (synchronized) by external time cues (zeitgebers), most notably the daily light/ dark and temperature cycles. The adaptive ability of circadian clocks to be reset by external cues enables organisms to maintain temporal alignment between their endogenously driven rhythms and biologically advantageous times in a daily cycle. A powerful strategy for probing this resetting feature is based on the ability of short pulses of environmental stimuli or other agents to elicit phase shifts in circadian pacemakers. These perturbation experiments revealed that the direction (i.e., delay or advance) and magnitude of a phase shift are functions of the time in a daily cycle that the zeitgeber is administered. Plotting the average phase shift as a function of time that the stimulus was applied yields a phase-response curve (PRC) that describes...

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Light-pulse phase response curves for the locomotor activity rhythm in Period mutants of Drosophila melanogaster

Cited by 74 publications

References 25 publications

per mRNA Cycling Is Locked to Lights-Off under Photoperiodic Conditions That Support Circadian Feedback Loop Function

per mRNA Cycling Is Locked to Lights-Off under Photoperiodic Conditions That Support Circadian Feedback Loop Function

Phase-Shifting the Fruit Fly Clock without Cryptochrome

Differential Effects of Light and Heat on the Drosophila Circadian Clock Proteins PER and TIM

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