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      Hypothalamic Proopiomelanocortin Is Necessary for Normal Glucose Homeostasis in Female Mice

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          Abstract

          The arcuate nucleus of the hypothalamus is a key regulator of energy balance and glucose homeostasis. In particular, arcuate proopiomelanocortin (POMC) neurons inhibit food intake, stimulate energy expenditure and increase glucose tolerance. The interruption of insulin or glucose signaling in POMC neurons leads to glucose intolerance without changing energy homeostasis. Although it was previously shown that POMC neurons are necessary for normal glucose homeostasis, the participation of POMC neuropeptide, by mechanisms independent of energy balance, remains to be demonstrated. To study the role of POMC in the regulation of glucose homeostasis, we performed glucose and insulin tolerance tests in non-obese mice lacking hypothalamic POMC expression. We found that POMC deficiency leads to glucose intolerance and insulin resistance in female mice before the onset of obesity or hyperphagia. Conversely, POMC deficiency does not impair glucose homeostasis in non-obese male mice. Interestingly, females completely normalize both glucose and insulin tolerance after genetic POMC restoration. Next, to further study sex dimorphism of POMC neurons regarding glucose homeostasis, we measured glucose-elicited changes in C-FOS by performing immunofluorescence in brain slices of POMC-EGFP mice. Remarkably, we found that glucose-induced C-FOS expression in POMC neurons is more than 3-fold higher in female than in male mice. Altogether, our results reveal a key role of arcuate POMC in the regulation of glucose homeostasis in females. Since POMC reactivation completely reverses the diabetogenic phenotype, arcuate POMC could be a potential target for diabetes therapy.

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          Most cited references17

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          Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity.

          A subset of neurons in the brain, known as 'glucose-excited' neurons, depolarize and increase their firing rate in response to increases in extracellular glucose. Similar to insulin secretion by pancreatic beta-cells, glucose excitation of neurons is driven by ATP-mediated closure of ATP-sensitive potassium (K(ATP)) channels. Although beta-cell-like glucose sensing in neurons is well established, its physiological relevance and contribution to disease states such as type 2 diabetes remain unknown. To address these issues, we disrupted glucose sensing in glucose-excited pro-opiomelanocortin (POMC) neurons via transgenic expression of a mutant Kir6.2 subunit (encoded by the Kcnj11 gene) that prevents ATP-mediated closure of K(ATP) channels. Here we show that this genetic manipulation impaired the whole-body response to a systemic glucose load, demonstrating a role for glucose sensing by POMC neurons in the overall physiological control of blood glucose. We also found that glucose sensing by POMC neurons became defective in obese mice on a high-fat diet, suggesting that loss of glucose sensing by neurons has a role in the development of type 2 diabetes. The mechanism for obesity-induced loss of glucose sensing in POMC neurons involves uncoupling protein 2 (UCP2), a mitochondrial protein that impairs glucose-stimulated ATP production. UCP2 negatively regulates glucose sensing in POMC neurons. We found that genetic deletion of Ucp2 prevents obesity-induced loss of glucose sensing, and that acute pharmacological inhibition of UCP2 reverses loss of glucose sensing. We conclude that obesity-induced, UCP2-mediated loss of glucose sensing in glucose-excited neurons might have a pathogenic role in the development of type 2 diabetes.
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            Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin.

            Pro-opiomelanocortin (POMC)-derived peptides (the melanocortins adrenocorticotropin, alpha-, beta- and gamma-melanocyte stimulating hormone; and the endogenous opioid beta-endorphin) have a diverse array of biological activities, including roles in pigmentation, adrenocortical function and regulation of energy stores, and in the immune system and the central and peripheral nervous systems. We show here that mice lacking the POMC-derived peptides have obesity, defective adrenal development and altered pigmentation. This phenotype is similar to that of the recently identified human POMC-deficient patients. When treated with a stable alpha-melanocyte-stimulating hormone agonist, mutant mice lost more than 40% of their excess weight after 2 weeks. Our results identify the POMC-null mutant mouse as a model for studying the human POMC-null syndrome, and indicate the therapeutic use of peripheral melanocortin in the treatment of obesity.
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              AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons.

              Hypothalamic AMP-activated protein kinase (AMPK) has been suggested to act as a key sensing mechanism, responding to hormones and nutrients in the regulation of energy homeostasis. However, the precise neuronal populations and cellular mechanisms involved are unclear. The effects of long-term manipulation of hypothalamic AMPK on energy balance are also unknown. To directly address such issues, we generated POMC alpha 2KO and AgRP alpha 2KO mice lacking AMPK alpha2 in proopiomelanocortin- (POMC-) and agouti-related protein-expressing (AgRP-expressing) neurons, key regulators of energy homeostasis. POMC alpha 2KO mice developed obesity due to reduced energy expenditure and dysregulated food intake but remained sensitive to leptin. In contrast, AgRP alpha 2KO mice developed an age-dependent lean phenotype with increased sensitivity to a melanocortin agonist. Electrophysiological studies in AMPK alpha2-deficient POMC or AgRP neurons revealed normal leptin or insulin action but absent responses to alterations in extracellular glucose levels, showing that glucose-sensing signaling mechanisms in these neurons are distinct from those pathways utilized by leptin or insulin. Taken together with the divergent phenotypes of POMC alpha 2KO and AgRP alpha 2KO mice, our findings suggest that while AMPK plays a key role in hypothalamic function, it does not act as a general sensor and integrator of energy homeostasis in the mediobasal hypothalamus.
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                Author and article information

                Contributors
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                19 September 2018
                2018
                : 9
                : 554
                Affiliations
                [1] 1Universidad de Buenos Aires, CONICET, Instituto de Fisiología y Biofísica “Bernardo Houssay” (IFIBIO), Grupo de Neurociencia de Sistemas , Buenos Aires, Argentina
                [2] 2Universidad de Buenos Aires, Facultad de Medicina, Departamento de Ciencias Fisiológicas , Buenos Aires, Argentina
                Author notes

                Edited by: Toru Hosoi, Hiroshima University, Japan

                Reviewed by: Guojun Shi, University of Michigan, United States; Miguel López, Universidade de Santiago de Compostela, Spain; Abhiram Sahu, University of Pittsburgh, United States

                *Correspondence: Viviana Florencia Bumaschny vbumaschny@ 123456fmed.uba.ar

                This article was submitted to Cellular Endocrinology, a section of the journal Frontiers in Endocrinology

                †These authors have contributed equally to this work

                Article
                10.3389/fendo.2018.00554
                6156137
                30283405
                259bad69-932f-41b5-8980-ebb40f4e881d
                Copyright © 2018 Alsina, Trotta and Bumaschny.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 28 March 2018
                : 30 August 2018
                Page count
                Figures: 3, Tables: 0, Equations: 0, References: 30, Pages: 7, Words: 4269
                Funding
                Funded by: Fundación Florencio Fiorini 10.13039/501100003074
                Award ID: Subsidios para Investigación en Ciencias Biomédicas año 2014
                Funded by: Agencia Nacional de Promoción Científica y Tecnológica 10.13039/501100003074
                Award ID: PICT 2014-2000
                Funded by: Consejo Nacional de Investigaciones Científicas y Técnicas 10.13039/501100002923
                Award ID: PIP 0487
                Funded by: Universidad de Buenos Aires 10.13039/501100005363
                Categories
                Endocrinology
                Brief Research Report

                Endocrinology & Diabetes
                proopiomelanocortin,glucose tolerance,insulin sensitivity,diabetes,hypothalamus,esr1

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