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      Chronic circadian advance shifts abolish melatonin secretion for days in rats

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          Abstract

          Melatonin deficiency has been proposed to underlie higher risks for cardiovascular and several other diseases in humans experiencing prolonged shiftwork. However, melatonin secretion has not been monitored longitudinally during consecutive shifts of the light:dark (LD) cycles in the same individuals (animals or humans) and the extent of melatonin deficiency is unknown in individuals experiencing consecutive LD shifts. We investigated the effect of consecutive LD shifts on melatonin secretion in adult F344 rats using continuous online pineal-microdialysis. The rats were entrained to the 12 h:12 h LD cycle before the shifts. The LD cycle was then advanced (n=5) or delayed (n=4) for six hours every four days for four consecutive times. The rats exhibited marked asymmetry in response to delay or advance LD shifts. While rats exposed to the repeated LD delay shifts always exhibited melatonin secretion throughout the entire periods, repeated LD advance shifts suppressed nocturnal melatonin secretion for several consecutive days in the middle of the 3-week period. Moreover, melatonin offset after LD delay and melatonin onset after LD advance determined the rate of circadian pacemaker reentrainment. Additionally, melatonin offset was phase locked at the new dark/light junctions for days following LD advance. These data demonstrate that chronic LD shifts are deleterious to melatonin rhythms, and that this effect is much more pronounced during advance shifts. These data may enhance our understanding of impact of LD shifts on our circadian timing system and benefit better design of shiftwork schedules to avoid melatonin disruption.

          Highlights

          • •

            Melatonin secretion differentially impacted by repeated delay versus advance shifts of the light:dark (LD) cycle in rats.

          • •

            Following two consecutive 6h advance shifts of LD cycle, melatonin disappeared for days.

          • •

            Repeated advance LD shifts are far more deleterious than repeated delay LD shifts.

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          Most cited references17

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          Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor.

          George Brainard, John Hanifin, Jeffrey M. Greeson … (2001)
          The photopigment in the human eye that transduces light for circadian and neuroendocrine regulation, is unknown. The aim of this study was to establish an action spectrum for light-induced melatonin suppression that could help elucidate the ocular photoreceptor system for regulating the human pineal gland. Subjects (37 females, 35 males, mean age of 24.5 +/- 0.3 years) were healthy and had normal color vision. Full-field, monochromatic light exposures took place between 2:00 and 3:30 A.M. while subjects' pupils were dilated. Blood samples collected before and after light exposures were quantified for melatonin. Each subject was tested with at least seven different irradiances of one wavelength with a minimum of 1 week between each nighttime exposure. Nighttime melatonin suppression tests (n = 627) were completed with wavelengths from 420 to 600 nm. The data were fit to eight univariant, sigmoidal fluence-response curves (R(2) = 0.81-0.95). The action spectrum constructed from these data fit an opsin template (R(2) = 0.91), which identifies 446-477 nm as the most potent wavelength region providing circadian input for regulating melatonin secretion. The results suggest that, in humans, a single photopigment may be primarily responsible for melatonin suppression, and its peak absorbance appears to be distinct from that of rod and cone cell photopigments for vision. The data also suggest that this new photopigment is retinaldehyde based. These findings suggest that there is a novel opsin photopigment in the human eye that mediates circadian photoreception.
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            Daily exercise facilitates phase delays of circadian melatonin rhythm in very dim light.

            Mary Barger, Anthony Wright, R. Hughes … (2004)
            Shift workers and transmeridian travelers are exposed to abnormal work-rest cycles, inducing a change in the phase relationship between the sleep-wake cycle and the endogenous circadian timing system. Misalignment of circadian phase is associated with sleep disruption and deterioration of alertness and cognitive performance. Exercise has been investigated as a behavioral countermeasure to facilitate circadian adaptation. In contrast to previous studies where results might have been confounded by ambient light exposure, this investigation was conducted under strictly controlled very dim light (standing approximately 0.65 lux; angle of gaze) conditions to minimize the phase-resetting effects of light. Eighteen young, fit males completed a 15-day randomized clinical trial in which circadian phase was measured in a constant routine before and after exposure to a week of nightly bouts of exercise or a nonexercise control condition after a 9-h delay in the sleep-wake schedule. Plasma samples collected every 30-60 min were analyzed for melatonin to determine circadian phase. Subjects who completed three 45-min bouts of cycle ergometry each night showed a significantly greater shift in the dim light melatonin onset (DLMO(25%)), dim light melatonin offset, and midpoint of the melatonin profile compared with nonexercising controls (Student t-test; P < 0.05). The magnitude of phase delay induced by the exercise intervention was significantly dependent on the relative timing of the exercise after the preintervention DLMO(25%) (r = -0.73, P < 0.05) such that the closer to the DLMO(25%), the greater the phase shift. These data suggest that exercise may help to facilitate circadian adaptation to schedules requiring a delay in the sleep-wake cycle.
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              Measuring Light at Night and Melatonin Levels in Shift Workers: A Review of the Literature.

              Claudia Hunter, Mariana G Figueiro (2017)
              Shift work, especially that involving rotating and night shifts, is associated with an increased risk of diseases, including cancer. Attempts to explain the association between shift work and cancer in particular have focused on the processes of melatonin production and suppression. One hypothesis postulates that exposure to light at night (LAN) suppresses melatonin, whose production is known to slow the development of cancerous cells, while another proposes that circadian disruption associated with shift work, and not just LAN, increases health risks. This review focuses on six studies that employed quantitative measurement of LAN and melatonin levels to assess cancer risks in shift workers. These studies were identified via searching the PubMed database for peer-reviewed, English-language articles examining the links between shift work, LAN, and disease using the terms light at night, circadian disruption, health, risk, cancer, shift work, or rotating shift. While the results indicate a growing consensus on the relationship between disease risks (particularly cancer) and circadian disruption associated with shift work, the establishment of a direct link between LAN and disease has been impeded by contradictory studies and a lack of consistent, quantitative methods for measuring LAN in the research to date. Better protocols for assessing personal LAN exposure are required, particularly those employing calibrated devices that measure and sample exposure to workplace light conditions, to accurately assess LAN's effects on the circadian system and disease. Other methodologies, such as measuring circadian disruption and melatonin levels in the field, may also help to resolve discrepancies in the findings.
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                Author and article information

                Contributors
                Jimo Borjigin
                Journal
                Journal ID (nlm-ta): Neurobiol Sleep Circadian Rhythms
                Journal ID (iso-abbrev): Neurobiol Sleep Circadian Rhythms
                Title: Neurobiology of Sleep and Circadian Rhythms
                Publisher: Elsevier
                ISSN (Electronic): 2451-9944
                Publication date PMC-release: 23 February 2018
                Publication date Collection: June 2018
                Publication date (Electronic): 23 February 2018
                Volume: 5
                Pages: 78-83
                Affiliations
                [a ]Department of Molecular and Integrative Physiology, University of Michigan, 1301 East Catherine Street, 7732C MS II, Ann Arbor, MI 48109-5622, USA
                [b ]Department of Neurology, University of Michigan, Ann Arbor, MI, USA
                [c ]Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI, USA
                Author notes
                [* ]Corresponding author at : Department of Molecular and Integrative Physiology, University of Michigan, 1301 East Catherine Street, 7732C MS II, Ann Arbor, MI 48109-5622, USA. borjigin@ 123456umich.edu
                [1]

                These two authors contributed equally.

                Article
                Publisher ID: S2451-9944(17)30035-4
                DOI: 10.1016/j.nbscr.2018.02.002
                PMC ID: 6584629
                SO-VID: b78368d4-d08e-4119-80d6-086dfe2f9647
                Copyright © © 2018 The Authors
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 8 December 2017
                Date revision received : 21 February 2018
                Date accepted : 22 February 2018
                Categories
                Subject: Research Paper

                Keywords: melatonin,chronic shift,phase delay,phase advance,shiftwork
                Data availability:
                Keywords: melatonin, chronic shift, phase delay, phase advance, shiftwork

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