Time-restricted feeding prevents deleterious metabolic effects of circadian disruption through epigenetic control of β cell function

Brown, Matthew; Sen, Satish; Mazzone, Amelia; Her, Tracy K.; Xiong, Yuning; Lee, Jeong‐Heon; Javeed, Naureen; Colwell, Christopher S.; Rakshit, Kuntol; LeBrasseur, Nathan K.; Gaspar-Maia, Alexandre; Ördög, Tamás; Matveyenko, Aleksey V.

doi:10.1126/sciadv.abg6856

Cited by 35 publications

(20 citation statements)

References 85 publications

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“…Still, we show here and have shown previously that reconstituted peripheral clocks can overcome this altered context, especially with the addition of night feeding ( 8 ). For example, though pancreas BMAL1 regulates glucose-stimulated insulin secretion from beta cells and is a key peripheral node of the clock system with respect to feeding-fasting behavior ( 27 , 28 ), night feeding of Liver+Muscle-RE mice induced a serum insulin rhythm and rescued systemic glucose tolerance even in the absence of pancreas BMAL1. In addition, central clock reconstituted mice also exhibit improved glucose tolerance, at least in part due to reinstated feeding-fasting behavior ( 7 ).…”

Section: Feeding Rhythms Bolster Autonomous Liver and Muscle Clocks E...mentioning

confidence: 99%

Interrogating Metabolic Interactions Between Skeletal Muscle and Liver Circadian Clocks In Vivo

Smith

Koronowski

Greco

et al. 2022

Preprint

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Expressed throughout the body, the circadian clock system achieves daily metabolic homeostasis at every level of physiology, with clock disruption associated with metabolic disease (1, 2). Molecular clocks present in the brain, liver, adipose, pancreas and skeletal muscle each contribute to glucose homeostasis (3). However, it is unclear; 1) which organ clocks provide the most essential contributions, and 2) if these contributions depend on inter-organ communication. We recently showed that the liver clock alone is insufficient for most aspects of daily liver glucose handling and requires connections with other clocks (4). Considering the pathways that link glucose metabolism between liver and skeletal muscle, we sought to test whether a clock connection along this axis is important. Using our previous published methodology for tissue-specific rescue of Bmal1 in vivo (4, 5), we now show that in the absence of feeding-fasting cycles, liver and muscle clocks are not sufficient for systemic glucose metabolism, nor do they form a functional connection influencing local glucose handling or daily transcriptional rhythms in each tissue. However, the introduction of a daily feeding-fasting rhythm enables a synergistic state between liver and muscle clocks that leads to restoration of systemic glucose tolerance. These findings reveal limited autonomous capabilities of liver and muscle clocks and highlight the need for inter-organ clock communication for glucose homeostasis which involves at least two peripheral metabolic organs.

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Section: Feeding Rhythms Bolster Autonomous Liver and Muscle Clocks E...mentioning

confidence: 99%

Interrogating Metabolic Interactions Between Skeletal Muscle and Liver Circadian Clocks In Vivo

Smith

Koronowski

Greco

et al. 2022

Preprint

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“…This is consistent with the latest systematic review and a cross-sectional study showing that evening chronotype was associated with a worse cardiometabolic risk profile and a higher risk of diabetes, cancer, and depression [ 44 , 45 ]. The latest research showed circadian rhythm disruption perturbed glucose homeostasis through disruption of pancreatic β cell function and loss of circadian transcriptional and epigenetic identity [ 46 ]. However, the opposite result was found in MR analysis, in which the IVW estimate yielded a morning chronotype and had an adverse effect on type 2 diabetes (OR = 1.37, 95% CI: 1.09–1.72, p = 0.0068).…”

Section: Discussionmentioning

confidence: 99%

Integrative Identification of Genetic Loci Jointly Influencing Diabetes-Related Traits and Sleep Traits of Insomnia, Sleep Duration, and Chronotypes

Zhou

et al. 2022

Biomedicines

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Accumulating evidence suggests a relationship between type 2 diabetes mellitus and sleep problems. A comprehensive study is needed to decipher whether shared polygenic risk variants exist between diabetic traits and sleep traits. Methods: We integrated summary statistics from different genome-wide association studies and investigated overlap in single-nucleotide polymorphisms (SNPs) associated with diabetes-related traits (type 2 diabetes, fasting glucose, fasting insulin, and glycated hemoglobin) and sleep traits (insomnia symptoms, sleep duration, and chronotype) using a conditional/conjunctional false discovery rate approach. Pleiotropic genes were further evaluated for differential expression analysis, and we assessed their expression pattern effects on type 2 diabetes by Mendelian randomization (MR) analysis. Results: We observed extensive polygenic pleiotropy between diabetic traits and sleep traits. Fifty-eight independent genetic loci jointly influenced the risk of type 2 diabetes and the sleep traits of insomnia, sleep duration, and chronotype. The strongest shared locus between type 2 diabetes and sleep straits was FTO (lead SNP rs8047587). Type 2 diabetes (z score, 16.19; P = 6.29 × 10−59) and two sleep traits, sleep duration (z score, −6.66; P = 2.66 × 10−11) and chronotype (z score, 7.42; P = 1.19 × 10−13), were shared. Two of the pleiotropic genes, ENSA and PMPCA, were validated to be differentially expressed in type 2 diabetes, and PMPCA showed a slight protective effect on type 2 diabetes in MR analysis. Conclusions: Our study provided evidence for the polygenic overlap between diabetic traits and sleep traits, of which the expression of PMPCA may play a crucial role and provide support of the hazardous effect of being an “evening” person on diabetes risk.

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“…Circadian disruption and shift work are environmental stressors characteristic of impaired feeding/fasting rhythms and have been directly linked to the development of islet failure in T2DM ( 22 , 162 ). Pancreatic islets isolated from circadian disrupted ( via constant light) mice exhibit complete ablation of circadian rhythms in both gene expression and chromatin accessibility ( 47 ). Providing further evidence that rhythmic feeding/fasting cycles drive islet transcription, tRF was shown to rescue transcriptional and epigenetic (chromatin accessibility) rhythms, despite global circadian disruption, of genes/loci annotated to pathways regulating circadian rhythms along with β-cell function (i.e., insulin secretion and exocytosis) and rest pathways (i.e., FoxO signaling, fatty acid metabolism) active during feeding and fasting, respectively.…”

Section: Islet Response To Time-dependent Regulation Of Food Intakementioning

confidence: 99%

“…This was followed by a series of studies demonstrating that "b-cell rest" or acute inhibition of insulin secretion, could restore b-cell function (first phase insulin secretion), insulin/Ca 2+ pulsatility, and insulin content in obesity and T2DM (144)(145)(146)(147)(148). Chronic bcell stimulation common to high fat feeding/obesity (149) and circadian disruption (21,22) result in both b-cell dysfunction and apoptosis which have been shown to be reversed by ADF (49,150), tRF (47,151,152), and a FMD (153). Specifically, a 12-week ADF regimen protected mice from HF diet induced b-cell dysfunction and failure (49), which was associated with enhanced GSIS, restored islet insulin content, and reduced apoptosis contingent on ADF activation of the autophagy-lysosome pathway.…”

Section: Islet Response To Time-dependent Regulation Of Food Intakementioning

confidence: 99%

It’s What and When You Eat: An Overview of Transcriptional and Epigenetic Responses to Dietary Perturbations in Pancreatic Islets

Brown

Matveyenko

2022

Front. Endocrinol.

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Our ever-changing modern environment is a significant contributor to the increased prevalence of many chronic diseases, and particularly, type 2 diabetes mellitus (T2DM). Although the modern era has ushered in numerous changes to our daily living conditions, changes in “what” and “when” we eat appear to disproportionately fuel the rise of T2DM. The pancreatic islet is a key biological controller of an organism’s glucose homeostasis and thus plays an outsized role to coordinate the response to environmental factors to preserve euglycemia through a delicate balance of endocrine outputs. Both successful and failed adaptation to dynamic environmental stimuli has been postulated to occur due to changes in the transcriptional and epigenetic regulation of pathways associated with islet secretory function and survival. Therefore, in this review we examined and evaluated the current evidence elucidating the key epigenetic mechanisms and transcriptional programs underlying the islet’s coordinated response to the interaction between the timing and the composition of dietary nutrients common to modern lifestyles. With the explosion of next generation sequencing, along with the development of novel informatic and –omic approaches, future work will continue to unravel the environmental-epigenetic relationship in islet biology with the goal of identifying transcriptional and epigenetic targets associated with islet perturbations in T2DM.

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Time-restricted feeding prevents deleterious metabolic effects of circadian disruption through epigenetic control of β cell function

Abstract: Time-restricted feeding improves glucose homeostasis through epigenetic control of pancreatic β cell function.

Cited by 35 publications

References 85 publications

Interrogating Metabolic Interactions Between Skeletal Muscle and Liver Circadian Clocks In Vivo

Interrogating Metabolic Interactions Between Skeletal Muscle and Liver Circadian Clocks In Vivo

Integrative Identification of Genetic Loci Jointly Influencing Diabetes-Related Traits and Sleep Traits of Insomnia, Sleep Duration, and Chronotypes

It’s What and When You Eat: An Overview of Transcriptional and Epigenetic Responses to Dietary Perturbations in Pancreatic Islets

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