Naturally-derived chronobiotics in chrononutrition

https://doi.org/10.1016/j.tifs.2019.11.020Get rights and content

Highlights

  • A disrupted circadian rhythm leads to various health problems.

  • Bioactive compounds can correct circadian disorders.

  • There is limited research about the chronobiotic effect of bioactive compounds.

  • Clinical trials evaluating the chronobiotics effects of compounds/foods are needed.

Abstract

Background

The circadian clock is an evolved autonomous timekeeping system that aligns body functions to the solar course, by anticipating/coordinating the required metabolic activities; such internal clock responds to several exogenous stimuli (Zeitgebers) able to synchronize the endogenous rhythm. A disrupted circadian rhythm leads to several neurodegenerative and metabolic illness such as obesity, diabetes, and psychiatric disorders.

Scope and approach

Circadian rhythm disorders have no current medical treatment, but chrononutrition has emerged as an important tool to enhance metabolic and nutritional health in sleep disorders. This review highlights the effects of meal timing, food types, nutrients and several bioactive xenobiotic compounds (chronobiotics) on circadian clocks. The potential application of diet therapies is discussed particularly to deal with certain metabolic disorders related to circadian misalignment.

Key findings and conclusions: The desynchronization of circadian rhythms negatively influences health necessitating the development of molecular modulators of circadian rhythms including food components, meal timing, or different diet types that can help correct circadian disorders attenuating the burden of chronic diseases. However, there is limited research on the chronobiotic effect of specific foods/compounds in clinical trials. Animal studies evaluating the chronobiological response, resulting from the ingestion of a particular food, are also limited; most available studies (in vitro and animal models) report the effect of a single nutrient (e.g., caffeine, palmitate, among others) which is difficult to translate to real-life situations. This review offers the perspective of a chronobiotic-based approach, identifying targets for health improvement, which are current lifestyle-associated issues.

Introduction

Every 24 h, the earth rotates once around its axis, exposing live organisms to predictable fluctuations of light and temperature. To optimally adjust their behavior, metabolism, and physiology living organisms developed an internal system called “circadian clock”. This clock has evolved as an autonomous timekeeping system that aligns behavioral patterns (including food intake) to daytime/nighttime and supports the body functions by anticipating and coordinating the required metabolic programs. The brain is the master organ controlling circadian rhythmicity by responding to environmental light and darkness cues called Zeitgebers (Reinke & Asher, 2019).

Each body cell is equipped with its circadian clock (a.k.a. oscillator) to achieve the timely homeostasis of the entire organism. This master clock confers rhythmicity by controlling rate-limiting steps in the cell's daily metabolic program (Kiehn et al., 2017, Reinke and Asher, 2019). Circadian rhythms, cycles with a recurrent periodicity also respond to Zeitgebers (Herzog, 2007), and are responsible for controlling different physiological processes such as sleep & wake cycles, body temperature, cardiovascular activity, hunger/appetite, endocrine hormone secretion, and renal function (Zee, Attarian, & Videnovic, 2013).

Disruption of the circadian clock by external (e.g. night shift-work or jet-lag) or internal desynchronization (e.g. nyctalopia, aging), negatively affects rest-to-activity cycles, leading to various health problems including individual psychiatric and metabolic disorders such as obesity, diabetes, hyperglycemia, and cancer (Pfeffer et al., 2018, Zee et al., 2013). For example, transient timing changes such as summer time changes are associated with increased risk of acute myocardial infarction (Tarquini, Carbone, Martinez, & Mazzoccoli, 2019). The physiologic disruption of circadian rhythms may also accelerate lung tumorigenesis (Papagiannakopoulos et al., 2016) by affecting its initiation-progression- metastasis continuum (Masri & Sassone-Corsi, 2018). Furthermore, experimental and clinical studies have consistently demonstrated that altering of circadian rhythms may enhance the development and progression of digestive pathologies, such as irritable bowel syndrome (IBS), and inflammatory bowel diseases (IBD), a fact linked to dysmotility or changes in microbiota composition (Codoñer-Franch & Gombert, 2018). Consequently, research has focused on chrono-therapeutic approaches, as an additive, and noninvasive treatment aid to deal with several illnesses; for example, bright light therapy (BLT), wake therapy, and sleep phase are used in the treatment of adult depression (Kirschbaum-Lesch, Holtmann, & Legenbauer, 2019).

The first part of this narrative review (Siddaway, Wood, & Hedges, 2019) relates to the metabolomics regulation of peripheral circadian clocks and their synchronization. The second part deals with evidence on the effects of specific nutrients/xenobiotics, all of them known as naturally-derived chronobiotics, in the chrononutrition area, and their relation with normal and abnormal metabolism and non-communicable chronic diseases (NCCD) such as cancer, liver diseases and insulin resistance.

Section snippets

Method

In selecting the search strategy and classification of the information included herein, the recommendations of Siddaway et al. (2019) were followed. Briefly, to ensure ‘state of the art’ scientific communications in the field of ‘chrononutrition’ and ‘chronobiotics’, a cursory search of articles' titles or abstracts (tiab) using these exact searching terms or their associated Medical Subject Heading (MeSH; https://meshb-prev.nlm.nih.gov/search) codes [circadian rhythm (MeSH D002940), circadian

History of the study of biological rhythms

Biological rhythms in plants and animals date from 5000 B.C. Hippocrates (1955, century IV B.C.) described the relation between biological rhythmicity, seasonality, time of day, and age with the incidence of some diseases (Fig. 1). In this era, Androsthenes of Thasos also described the cyclical opening of the tamarind plant (Bretzl, 1903); however, Sanctorius was the first to design a “chronobiology laboratory” in 1657 and use an “autorhytmometric method” in 1711 (Reinberg & Smolensky, 1983).

Regulation of the master and peripheral clocks

Circadian rhythms are generated endogenously and regulated by a master or central clock located in the suprachiasmatic nucleus (SCN), in the anterior hypothalamus of mammals. The SCN contains approximately 15–20,000 neurons which have the remarkable feature of oscillating with a 24 h based rhythm. However, they do not function in isolation from their surroundings; instead, they are entrained by external cues. Light has been described as the most potent synchronizer in humans, allowing us to

Food as synchronizers of peripheral clocks

British adults with more irregular food consumption, especially during breakfast and between meals, showed increased cardiometabolic risk, as well as a higher risk of obesity and metabolic syndrome, despite consuming less energy (Pot, Hardy, & Stephen, 2014). However, the study did not evaluate the relationship of diet characteristics (mealtime and food consumption) and the circadian rhythm suggested as determinants of the circadian rhythm synchronization that can directly influence metabolic

Influence of nutrients on circadian rhythms and clock gene expression in different tissues

Single nutrients such as sodium, amino acids, caffeine, cinnamic acid, nobiletin, palmitate, theophylline, thiamine, ethanol, and retinoic acid can reset or phase-shift circadian rhythms according to in vitro or animal studies (Fig. 3) (Froy, 2007; Oike, 2017). For instance, glucose can activate circadian gene expression of Per1, Per2, and Bmal1 suggesting a role in the synchronization of central and peripheral clocks (Oosterman et al., 2014). Amino acids have also been reported as circadian

Gut microbiota and peripheral clocks

Microbiome plays an essential role in regulating many physiological processes including digestion of food components, host metabolism, immune system, epithelial homeostasis, host behavior, and cognitive function (Mukherji, Kobiita, Ye, & Chambon, 2013). Interestingly, gut microbiota also influences the circadian clock, displaying circadian oscillations, characterized by day-night changes in composition or function of the intestinal microbiome, and its interaction with the host can also affect

Sleep efficiency

Sleep loss has recently been recognized as a public health concern increasingly prevalent in our society. A third of the United States population obtains insufficient regular sleep, with adverse health consequences including metabolic and mental disorders affecting human physiology and behavior (Liu, 2016). Sleep loss has also been associated with deficits in attention, cognition, metabolism, hormonal balance, mood, and cardiovascular function (Aguirre, 2016).

The intake of Jerte Valley cherries

Ingenuity/knowledge gap

The desynchronization of the circadian rhythms either in the central clock or one of the peripheral clocks can be caused by external or internal cues, adversely impacting various diseases particularly related to metabolic and neurological problems. This necessitates the development of molecular modulators of circadian rhythms, for example food components such as bioactive compounds, specific feeding schedules or different diet types. The evidence suggests that bioactive compounds can correct

Declaration of competing interest

The authors report no conflicts of interest.

Acknowledgements

Author E. Dufoo-Hurtado thanks the Consejo Nacional de Ciencia y Tecnología (CONACYT-Mexico) for the support of a Ph D. scholarship (779172). The authors would like to thank Dr. Mario Enrique Rodríguez García (Universidad Nacional Autónoma de México, Centro de Física Aplicada y Tecnología Avanzada, México), and Dr. B. Dave Oomah (Retired; Agriculture and Agri-Food Canada, Summerland, British Columbia, Canada) for their valuable support to this paper.

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