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      Curcumin prevents neuronal loss and structural changes in the superior cervical (sympathetic) ganglion induced by chronic sleep deprivation, in the rat model

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          Abstract

          Background

          In modern societies, sleep deprivation is a serious health problem. This problem could be induced by a variety of reasons, including lifestyle habits or neurological disorders. Chronic sleep deprivation (CSD) could have complex biological consequences, such as changes in neural autonomic control, increased oxidative stress, and inflammatory responses. The superior cervical ganglion (SCG) is an important sympathetic component of the autonomic nervous system. CSD can lead to a wide range of neurological consequences in SCG, which mainly supply innervations to circadian system and other structures. As the active component of Curcuma longa, curcumin possesses many therapeutic properties; including neuroprotective. This study aimed to evaluate the effect of CSD on the SCG histomorphometrical changes and the protective effect of curcumin in preventing these changes.

          Methods

          Thirty-six male rats were randomly assigned to the control, curcumin, CSD, CSD + curcumin, grid floor control, and grid floor + curcumin groups. The CSD was induced by a modified multiple platform apparatus for 21 days and animals were sacrificed at the end of CSD or treatment, and their SCGs removed for stereological and TUNEL evaluations and also spatial arrangement of neurons in this structure.

          Results

          Concerning stereological findings, CSD significantly reduced the volume of SCG and its total number of neurons and satellite glial cells in comparison with the control animals ( P < 0.05). Treatment of CSD with curcumin prevented these decreases. Furthermore, TUNEL evaluation showed significant apoptosis in the SCG cells in the CSD group, and treatment with curcumin significantly decreased this apoptosis ( P < 0.01). This decrease in apoptosis was observed in all control groups that received curcumin. CSD also changed the spatial arrangement of ganglionic neurons into a random pattern, whereas treatment with curcumin preserved its regular pattern.

          Conclusions

          CSD could potentially induce neuronal loss and structural changes including random spatial distribution in the SCG neurons. Deleterious effects of sleep deprivation could be prevented by the oral administration of curcumin. Furthermore, the consumption of curcumin in a healthy person might lead to a reduction of cell death.

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          Most cited references62

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          Sleep deprivation as a neurobiologic and physiologic stressor: Allostasis and allostatic load.

          Sleep has important homeostatic functions, and sleep deprivation is a stressor that has consequences for the brain, as well as many body systems. Whether sleep deprivation is due to anxiety, depression, or a hectic lifestyle, there are consequences of chronic sleep deprivation that impair brain functions and contribute to allostatic load throughout the body. Allostatic load refers to the cumulative wear and tear on body systems caused by too much stress and/or inefficient management of the systems that promote adaptation through allostasis. Chronic sleep deprivation in young healthy volunteers has been reported to increase appetite and energy expenditure, increase levels of proinflammatory cytokines, decrease parasympathetic and increase sympathetic tone, increase blood pressure, increase evening cortisol levels, as well as elevate insulin and blood glucose. Repeated stress in animal models causes brain regions involved in memory and emotions, such as hippocampus, amygdala, and prefrontal cortex, to undergo structural remodeling with the result that memory is impaired and anxiety and aggression are increased. Structural and functional magnetic resonance imaging studies in depression and Cushing's disease, as well as anxiety disorders, provide evidence that the human brain may be similarly affected. Moreover, brain regions such as the hippocampus are sensitive to glucose and insulin, and both type 1 and type 2 diabetes mellitus are associated with cognitive impairment and (for type 2 diabetes mellitus) increased risk for Alzheimer's disease. Animal models of chronic sleep deprivation indicate that memory is impaired along with depletion of glycogen stores and increases in oxidative stress and free radical production. Taken together, these changes in brain and body are further evidence that sleep deprivation is a chronic stressor and that the resulting allostatic load can contribute to cognitive problems, which can, in turn, further exacerbate pathways that lead to disease.
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            Role of sleep and circadian disruption on energy expenditure and in metabolic predisposition to human obesity and metabolic disease.

            Weight gain, obesity and diabetes have reached alarming levels in the developed world. Traditional risk factors such as over-eating, poor nutritional choices and lack of exercise cannot fully account for the high prevalence of metabolic disease. This review paper examines the scientific evidence on two novel risk factors that contribute to dys-regulated metabolic physiology: sleep disruption and circadian misalignment. Specifically, fundamental relationships between energy metabolism and sleep and circadian rhythms and the impact of sleep and circadian disruption on metabolic physiology are examined. Millions of individuals worldwide do not obtain sufficient sleep for healthy metabolic function, and many participate in shift work and social activities at times when the internal physiological clock is promoting sleep. These behaviours predispose an individual for poor metabolic health by promoting excess caloric intake in response to reduced sleep, food intake at internal biological times when metabolic physiology is not prepared, decreased energy expenditure when wakefulness and sleep are initiated at incorrect internal biological times, and disrupted glucose metabolism during short sleep and circadian misalignment. In addition to the traditional risk factors of poor diet and exercise, disturbed sleep and circadian rhythms represent modifiable risk factors for prevention and treatment of metabolic disease and for promotion of healthy metabolism.
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              Breast cancer and circadian disruption from electric lighting in the modern world.

              Breast cancer is the leading cause of cancer death among women worldwide, and there is only a limited explanation of why. Risk is highest in the most industrialized countries but also is rising rapidly in the developing world. Known risk factors account for only a portion of the incidence in the high-risk populations, and there has been considerable speculation and many false leads on other possibly major determinants of risk, such as dietary fat. A hallmark of industrialization is the increasing use of electricity to light the night, both within the home and without. It has only recently become clear that this evolutionarily new and, thereby, unnatural exposure can disrupt human circadian rhythmicity, of which three salient features are melatonin production, sleep, and the circadian clock. A convergence of research in cells, rodents, and humans suggests that the health consequences of circadian disruption may be substantial. An innovative experimental model has shown that light at night markedly increases the growth of human breast cancer xenografts in rats. In humans, the theory that light exposure at night increases breast cancer risk leads to specific predictions that are being tested epidemiologically: evidence has accumulated on risk in shift workers, risk in blind women, and the impact of sleep duration on risk. If electric light at night does explain a portion of the breast cancer burden, then there are practical interventions that can be implemented, including more selective use of light and the adoption of recent advances in lighting technology and application. © 2013 American Cancer Society, Inc.
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                Author and article information

                Contributors
                noora@sums.ac.ir
                namavarreza@yahoo.com
                Journal
                Biol Res
                Biol. Res
                Biological Research
                BioMed Central (London )
                0716-9760
                0717-6287
                10 July 2020
                10 July 2020
                2020
                : 53
                : 31
                Affiliations
                [1 ]GRID grid.412571.4, ISNI 0000 0000 8819 4698, Department of Anatomical Sciences, School of Medicine, , Shiraz University of Medical Sciences, ; Shiraz, Iran
                [2 ]GRID grid.412571.4, ISNI 0000 0000 8819 4698, Histomorphometry and Stereology Research Centre, Shiraz University of Medical Sciences, ; 71348-45794 Shiraz, Iran
                [3 ]GRID grid.412571.4, ISNI 0000 0000 8819 4698, Clinical Neurology Research Center, , Shiraz University of Medical Sciences, ; 71348-45794 Shiraz, Iran
                [4 ]GRID grid.412571.4, ISNI 0000 0000 8819 4698, Laboratory for Stem Cell Research, Department of Anatomical Sciences, , Shiraz University of Medical Sciences, ; Shiraz, Iran
                Author information
                http://orcid.org/0000-0002-6635-2717
                Article
                300
                10.1186/s40659-020-00300-8
                7350621
                32650839
                a0d0fe8e-315c-4625-beb5-45dc81511a36
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 24 February 2020
                : 6 July 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004320, Shiraz University of Medical Sciences;
                Award ID: 95-01-01-13637
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                chronic sleep deprivation,superior cervical ganglion,curcumin,stereology,apoptosis,spatial arrangement of neurons

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