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      Estrogen- and Satiety State-Dependent Metabolic Lateralization in the Hypothalamus of Female Rats

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          Abstract

          Hypothalamus is the highest center and the main crossroad of numerous homeostatic regulatory pathways including reproduction and energy metabolism. Previous reports indicate that some of these functions may be driven by the synchronized but distinct functioning of the left and right hypothalamic sides. However, the nature of interplay between the hemispheres with regard to distinct hypothalamic functions is still unclear. Here we investigated the metabolic asymmetry between the left and right hypothalamic sides of ovariectomized female rats by measuring mitochondrial respiration rates, a parameter that reflects the intensity of cell and tissue metabolism. Ovariectomized (saline injected) and ovariectomized+estrogen injected animals were fed ad libitum or fasted to determine 1) the contribution of estrogen to metabolic asymmetry of hypothalamus; and 2) whether the hypothalamic asymmetry is modulated by the satiety state. Results show that estrogen-priming significantly increased both the proportion of animals with detected hypothalamic lateralization and the degree of metabolic difference between the hypothalamic sides causing a right-sided dominance during state 3 mitochondrial respiration (St3) in ad libitum fed animals. After 24 hours of fasting, lateralization in St3 values was clearly maintained; however, instead of the observed right-sided dominance that was detected in ad libitum fed animals here appeared in form of either right- or left-sidedness. In conclusion, our results revealed estrogen- and satiety state-dependent metabolic differences between the two hypothalamic hemispheres in female rats showing that the hypothalamic hemispheres drive the reproductive and satiety state related functions in an asymmetric manner.

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          Most cited references 40

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          Hypothalamic Sirt1 Regulates Food Intake in a Rodent Model System

          Sirt1 is an evolutionarily conserved NAD+ dependent deacetylase involved in a wide range of processes including cellular differentiation, apoptosis, as well as metabolism, and aging. In this study, we investigated the role of hypothalamic Sirt1 in energy balance. Pharmacological inhibition or siRNA mediated knock down of hypothalamic Sirt1 showed to decrease food intake and body weight gain. Central administration of a specific melanocortin antagonist, SHU9119, reversed the anorectic effect of hypothalamic Sirt1 inhibition, suggesting that Sirt1 regulates food intake through the central melanocortin signaling. We also showed that fasting increases hypothalamic Sirt1 expression and decreases FoxO1 (Forkhead transcription factor) acetylation suggesting that Sirt1 regulates the central melanocortin system in a FoxO1 dependent manner. In addition, hypothalamic Sirt1 showed to regulate S6K signaling such that inhibition of the fasting induced Sirt1 activity results in up-regulation of the S6K pathway. Thus, this is the first study providing a novel role for the hypothalamic Sirt1 in the regulation of food intake and body weight. Given the role of Sirt1 in several peripheral tissues and hypothalamus, potential therapies centered on Sirt1 regulation might provide promising therapies in the treatment of metabolic diseases including obesity.
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            Antiphase oscillation of the left and right suprachiasmatic nuclei.

            An unusual property of the circadian timekeeping systems of animals is rhythm "splitting," in which a single daily period of physical activity (usually measured as wheel running) dissociates into two stably coupled components about 12 hours apart; this behavior has been ascribed to a clock composed of two circadian oscillators cycling in antiphase. We analyzed gene expression in the hypothalamic circadian clock, the suprachiasmatic nucleus (SCN), of behaviorally "split" hamsters housed in constant light. The results show that the two oscillators underlying the split condition correspond to the left and right sides of the bilaterally paired SCN.
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              Abnormal Asymmetry of Brain Connectivity in Schizophrenia

              Recently, a growing body of data has revealed that beyond a dysfunction of connectivity among different brain areas in schizophrenia patients (SCZ), there is also an abnormal asymmetry of functional connectivity compared with healthy subjects. The loss of the cerebral torque and the abnormalities of gyrification, with an increased or more complex cortical folding in the right hemisphere may provide an anatomical basis for such aberrant connectivity in SCZ. Furthermore, diffusion tensor imaging studies have shown a significant reduction of leftward asymmetry in some key white-matter tracts in SCZ. In this paper, we review the studies that investigated both structural brain asymmetry and asymmetry of functional connectivity in healthy subjects and SCZ. From an analysis of the existing literature on this topic, we can hypothesize an overall generally attenuated asymmetry of functional connectivity in SCZ compared to healthy controls. Such attenuated asymmetry increases with the duration of the disease and correlates with psychotic symptoms. Finally, we hypothesize that structural deficits across the corpus callosum may contribute to the abnormal asymmetry of intra-hemispheric connectivity in schizophrenia.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 September 2015
                2015
                : 10
                : 9
                Affiliations
                [1 ]Department of Physiology and Biochemistry, Szent Istvan University Faculty of Veterinary Science, Budapest, Hungary
                [2 ]Department of Transplantation and Surgery, Semmelweis University, Budapest, Hungary
                [3 ]Division of Comparative Medicine, Yale University School of Medicine, New Haven, CT, United States of America
                [4 ]Department of Animal Physiology and Animal Health, Szent Istvan University Faculty of Agricultural and Environmental Sciences, Godollo, Hungary
                Hosptial Infantil Universitario Niño Jesús, CIBEROBN, SPAIN
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: IT DSK AZ. Performed the experiments: GJ VS IT DSK. Analyzed the data: TB LVF ET. Contributed reagents/materials/analysis tools: ET. Wrote the paper: IT DSK AZ TH.

                Article
                PONE-D-15-30826
                10.1371/journal.pone.0137462
                4560379
                26339901

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Page count
                Figures: 3, Tables: 0, Pages: 11
                Product
                Funding
                This work was supported by OTKA 104982 (Nemzeti Kutatási, Fejlesztési és Innovációs Hivatal; http://www.otka.hu/) to AZ, and OTKA 72186 (Nemzeti Kutatási, Fejlesztési és Innovációs Hivatal; http://www.otka.hu/) to TB (design, data collection, analysis); NKB 15930, KK UK-12021 (Faculty of Veterinary Science; http://www.univet.hu/hu/kiemelt-egysegek/tkk/palyazatok-kutato-kar-2013-16/kutato-kar/) (data collection); KK PhD-15263 (Faculty of Veterinary Science; http://www.univet.hu/hu/kiemelt-egysegek/tkk/palyazatok-kutato-kar-2013-16/kutato-kar/) (preparation of the manuscript); and 9877-3/2015/FEKUT (grant of the Hungarian Ministry of Human Resources) (preparation of manuscript).
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