Rapidly alternating photoperiods disrupt central and peripheral rhythmicity and decrease plasma glucose, but do not affect glucose tolerance or insulin secretion in sheep

Abstract

New Findings r What is the central question of this study?Disrupting circadian rhythms in rodents perturbs glucose metabolism and increases adiposity. In this study, we asked whether circadian rhythm disruption, induced by exposure of sheep to rapidly alternating photoperiods (RAPs), also disrupts metabolic homeostasis in a large diurnal animal model. r What is the main finding and its importance?Exposure to RAPs disrupted central (melatonin and core body temperature) and peripheral rhythmicity (skeletal muscle clock gene expression). This led to reduced nocturnal plasma glucose concentrations, but did not affect glucose tolerance and glucose-stimulated insulin secretion. These results suggest that RAP-induced circadian rhythm disruption has minimal effect on glucose homeostasis in the sheep.Disrupting circadian rhythms in rodents perturbs glucose metabolism and increases adiposity. To determine whether these effects occur in a large diurnal animal, we assessed the impact of circadian rhythm disruption upon metabolic function in sheep. Adult ewes (n = 7) underwent 3 weeks of a control 12 h light-12 h dark photoperiod, followed by 4 weeks of rapidly alternating photoperiods (RAPs) whereby the time of light exposure was reversed twice each week. Measures of central (melatonin secretion and core body temperature) and peripheral rhythmicity (clock and metabolic gene expression in skeletal muscle) were obtained over 24 h in both conditions. Metabolic homeostasis was assessed by glucose tolerance tests and 24 h glucose and insulin profiles. Melatonin and core body temperature rhythms resynchronized within 2 days of the last photoperiod shift. High-amplitude Bmal1, Clock, Nr1d1, Cry2 and Per3 mRNA rhythms were apparent in skeletal muscle, which were phase advanced by up to 3.5 h at 2 days after the last phase shift, whereas Per1 expression was downregulated at this time. Pparα, Pgc1α and Nampt mRNA were constitutively expressed in both conditions. Nocturnal glucose concentrations were reduced following chronic phase shifts (zeitgeber time 0, −5.5%; zeitgeber time 12, −2.9%; and zeitgeber time 16, −5.7%), whereas plasma insulin, glucose tolerance and glucose-stimulated

Simulated shift work disrupts maternal circadian rhythms and metabolism, and increases gestation length in sheep

“…glucose tolerance tests (IVGTT) (0.25 g glucose kg –1 body weight) (Varcoe et al . ). Catheters were removed following IVGTT.…”

“…Therefore, in the present study, we investigated the effects of manipulating photoperiod and feeding time as a model of rotating shift schedules (Varcoe et al . ) with respect to behavioural, hormonal and molecular circadian rhythms, maternal metabolic health, and pregnancy outcomes in sheep.…”

Nutrition in the spotlight: metabolic effects of environmental light

“…In rats, however, the effects of repeated LD shifts seem to be Proceedings of the Nutrition Society strain dependent; in Long Evans (86) and Sprague Dawley (78) rats, repeated shifts do not affect body weight, whereas in F344 (87) and diabetes-prone human islet amyloid polypeptide rats (78) , repeated shifts do cause increased body weight gain. In sheep, representing a larger diurnal mammal, repeated LD shifts did not affect body weight or glucose tolerance (88) . Currently, repeated LD shifts are often used as a rodent model for shift-work in human subjects, a condition known to affect body weight and energy metabolism.…”

Disrupting the circadian photo-period alters the release of follicle-stimulating hormone, luteinizing hormone, progesterone, and estradiol in maternal and fetal sheep

“…In mammals, hormone secretion throughout pregnancy is also closely related to the circadian photo-period [23, 24]. For example, disrupting the circadian photo-period in sheep perturbs glucose metabolism and prolactin secretion during pregnancy [23, 24].…”

“…For example, disrupting the circadian photo-period in sheep perturbs glucose metabolism and prolactin secretion during pregnancy [23, 24]. However, to date, there is limited information regarding the effects of photo-period disruption in pregnancy on maternal and fetal reproductive hormone secretion.…”