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Neuroendocrine Control of Energy Metabolism

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A special issue of Metabolites (ISSN 2218-1989). This special issue belongs to the section "Endocrinology and Clinical Metabolic Research".

Deadline for manuscript submissions: closed (31 October 2021) | Viewed by 49020

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Special Issue Editors

Prof. Dr. Giancarlo Panzica

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Guest Editor

Department of Neuroscience “Rita Levi Montalcini”, University of Turin, I-10126 Turin, Italy
Interests: hypothalamus; metabolism disrupting chemicals; reproduction and metabolism; brain sex differences; endocrine disruptors
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Prof. Dr. Stefano Gotti

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Guest Editor

Department of Neuroscience “Rita Levi Montalcini”, University of Turin, I-10126 Turin, Italy
Interests: endocrine disruptors; brain sex differences; feeding brain circuits; anorexia nervosa; neuropeptides
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Paloma Collado Guirao

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Guest Editor

Dept. Psycobiology, Universidad Nacional de Education a Distancia (UNED), 28040 Madrid, Spain
Interests: energy metabolism programming; metabolic sex differences; sex steroids and feeding; feeding brain circuits; obesity and anorexia

Special Issue Information

Dear Colleagues,

The control of energy metabolism is a central event for cell, organ, and organism survival. There are many control levels in energy metabolism, but in this Special Issue, we will concentrate on the neuroendocrine control that is operated through specialized neural (mainly, but not exclusively, hypothalamic) circuits controlling both food intake and energy expenditure. Due to the explosion of obesity and related diseases, the subject of this Special Issue is of particular interest today.

The topics that will be covered by this Special Issue include but are not limited to:

Programming of neurohormonal circuits of feeding
Gut–brain axis and metabolic control
Neuropeptide systems in feeding behavior
Neural control of food reward
Eating disorders
Glial cells and neuroendocrine control
Adipose tissue and metabolic neural control
Gonadal hormones and feeding
Metabolic sex differences
Endocrine disruptors and neural control of feeding and energy metabolism

Manuscripts dealing with other pertinent challenging issues are also highly desired.

Prof. Giancarlo Panzica
Prof. Stefano Gotti
Prof. Paloma Collado Guirao
Guest Editors

Manuscript Submission Information

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Keywords

Hypothalamus
Sex differences
Feeding behavior
Endocrine disruptors
Energy metabolism
Neuroendocrine control
Eating disorders

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Published Papers (12 papers)

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Research

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25 pages, 4425 KiB

Open AccessArticle

The Crowded Uterine Horn Mouse Model for Examining Postnatal Metabolic Consequences of Intrauterine Growth Restriction vs. Macrosomia in Siblings

by Julia A. Taylor, Benjamin L. Coe, Toshi Shioda and Frederick S. vom Saal

Metabolites 2022, 12(2), 102; https://doi.org/10.3390/metabo12020102 - 22 Jan 2022

Cited by 2 | Viewed by 3671

Abstract

Differential placental blood flow and nutrient transport can lead to both intrauterine growth restriction (IUGR) and macrosomia. Both conditions can lead to adult obesity and other conditions clustered as metabolic syndrome. We previously showed that pregnant hemi-ovariectomized mice have a crowded uterine horn, resulting in siblings whose birth weights differ by over 100% due to differential blood flow based on uterine position. We used this crowded uterus model to compare IUGR and macrosomic male mice and also identified IUGR males with rapid (IUGR-R) and low (IUGR-L) postweaning weight gain. At week 12 IUGR-R males were heavier than IUGR-L males and did not differ from macrosomic males. Rapid growth in IUGR-R males led to glucose intolerance compared to IUGR-L males and down-regulation of adipocyte signaling pathways for fat digestion and absorption and type II diabetes. Macrosomia led to increased fat mass and altered adipocyte size distribution compared to IUGR males, and down-regulation of signaling pathways for carbohydrate and fat digestion and absorption relative to IUGR-R. Clustering analysis of gonadal fat transcriptomes indicated more similarities than differences between IUGR-R and macrosomic males compared to IUGR-L males. Our findings suggest two pathways to adult metabolic disease: macrosomia and IUGR with rapid postweaning growth rate. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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22 pages, 3905 KiB

Open AccessArticle

Distinct Changes in Gut Microbiota Are Associated with Estradiol-Mediated Protection from Diet-Induced Obesity in Female Mice

by Kalpana D. Acharya, Hye L. Noh, Madeline E. Graham, Sujin Suk, Randall H. Friedline, Cesiah C. Gomez, Abigail E. R. Parakoyi, Jun Chen, Jason K. Kim and Marc J. Tetel

Metabolites 2021, 11(8), 499; https://doi.org/10.3390/metabo11080499 - 30 Jul 2021

Cited by 13 | Viewed by 4568

Abstract

A decrease in ovarian estrogens in postmenopausal women increases the risk of weight gain, cardiovascular disease, type 2 diabetes, and chronic inflammation. While it is known that gut microbiota regulates energy homeostasis, it is unclear if gut microbiota is associated with estradiol regulation of metabolism. In this study, we tested if estradiol-mediated protection from high-fat diet (HFD)-induced obesity and metabolic changes are associated with longitudinal alterations in gut microbiota in female mice. Ovariectomized adult mice with vehicle or estradiol (E2) implants were fed chow for two weeks and HFD for four weeks. As reported previously, E2 increased energy expenditure, physical activity, insulin sensitivity, and whole-body glucose turnover. Interestingly, E2 decreased the tight junction protein occludin, suggesting E2 affects gut epithelial integrity. Moreover, E2 increased Akkermansia and decreased Erysipleotrichaceae and Streptococcaceae. Furthermore, Coprobacillus and Lactococcus were positively correlated, while Akkermansia was negatively correlated, with body weight and fat mass. These results suggest that changes in gut epithelial barrier and specific gut microbiota contribute to E2-mediated protection against diet-induced obesity and metabolic dysregulation. These findings provide support for the gut microbiota as a therapeutic target for treating estrogen-dependent metabolic disorders in women. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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27 pages, 4344 KiB

Open AccessArticle

Early Postnatal Genistein Administration Affects Mice Metabolism and Reproduction in a Sexually Dimorphic Way

by Marilena Marraudino, Giovanna Ponti, Chantal Moussu, Alice Farinetti, Elisabetta Macchi, Paolo Accornero, Stefano Gotti, Paloma Collado, Matthieu Keller and Giancarlo Panzica

Metabolites 2021, 11(7), 449; https://doi.org/10.3390/metabo11070449 - 10 Jul 2021

Cited by 7 | Viewed by 3839

Abstract

The phytoestrogen genistein (GEN) may interfere with permanent morphological changes in the brain circuits sensitive to estrogen. Due to the frequent use of soy milk in the neonatal diet, we aimed to study the effects of early GEN exposure on some physiological and reproductive parameters. Mice of both sexes from PND1 to PND8 were treated with GEN (50 mg/kg body weight, comparable to the exposure level in babies fed with soy-based formulas). When adult, we observed, in GEN-treated females, an advanced pubertal onset and an altered estrous cycle, and, in males, a decrease of testicle weight and fecal testosterone concentration. Furthermore, we observed an increase in body weight and altered plasma concentrations of metabolic hormones (leptin, ghrelin, triiodothyronine) limited to adult females. Exposure to GEN significantly altered kisspeptin and POMC immunoreactivity only in females and orexin immunoreactivity in both sexes. In conclusion, early postnatal exposure of mice to GEN determines long-term sex-specific organizational effects. It impairs the reproductive system and has an obesogenic effect only in females, which is probably due to the alterations of neuroendocrine circuits controlling metabolism; thus GEN, should be classified as a metabolism disrupting chemical. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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15 pages, 3480 KiB

Open AccessEditor’s ChoiceArticle

Hypothalamic Expression of Neuropeptide Y (NPY) and Pro-OpioMelanoCortin (POMC) in Adult Male Mice Is Affected by Chronic Exposure to Endocrine Disruptors

by Marilena Marraudino, Elisabetta Bo, Elisabetta Carlini, Alice Farinetti, Giovanna Ponti, Isabella Zanella, Diego Di Lorenzo, Gian Carlo Panzica and Stefano Gotti

Metabolites 2021, 11(6), 368; https://doi.org/10.3390/metabo11060368 - 9 Jun 2021

Cited by 11 | Viewed by 3878

Abstract

In the arcuate nucleus, neuropeptide Y (NPY) neurons, increase food intake and decrease energy expenditure, and control the activity of pro-opiomelanocortin (POMC) neurons, that decrease food intake and increase energy expenditure. Both systems project to other hypothalamic nuclei such as the paraventricular and dorsomedial hypothalamic nuclei. Endocrine disrupting chemicals (EDCs) are environmental contaminants that alter the endocrine system causing adverse health effects in an intact organism or its progeny. We investigated the effects of long-term exposure to some EDCs on the hypothalamic NPY and POMC systems of adult male mice that had been previously demonstrated to be a target of some of these EDCs after short-term exposure. Animals were chronically fed for four months with a phytoestrogen-free diet containing two different concentrations of bisphenol A, diethylstilbestrol, tributyltin, or E₂. At the end, brains were processed for NPY and POMC immunohistochemistry and quantitatively analyzed. In the arcuate and dorsomedial nuclei, both NPY and POMC immunoreactivity showed a statistically significant decrease. In the paraventricular nucleus, only the NPY system was affected, while the POMC system was not affected. Finally, in the VMH the NPY system was affected whereas no POMC immunoreactive material was observed. These results indicate that adult exposure to different EDCs may alter the hypothalamic circuits that control food intake and energy metabolism. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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11 pages, 1769 KiB

Open AccessArticle

Genistein during Development Alters Differentially the Expression of POMC in Male and Female Rats

by Jose Manuel Fernandez-Garcia, Beatriz Carrillo, Patricia Tezanos, Paloma Collado and Helena Pinos

Metabolites 2021, 11(5), 293; https://doi.org/10.3390/metabo11050293 - 2 May 2021

Cited by 5 | Viewed by 2636

Abstract

Phytoestrogens are considered beneficial for health, but some studies have shown that they may cause adverse effects. This study investigated the effects of genistein administration during the second week of life on energy metabolism and on the circuits regulating food intake. Two different genistein doses, 10 or 50 µg/g, were administered to male and female rats from postnatal day (P) 6 to P13. Physiological parameters, such as body weight and caloric intake, were then analyzed at P90. Moreover, proopiomelanocortin (POMC) expression in the arcuate nucleus (Arc) and orexin expression in the dorsomedial hypothalamus (DMH), perifornical area (PF) and lateral hypothalamus (LH) were studied. Our results showed a delay in the emergence of sex differences in the body weight in the groups with higher genistein doses. Furthermore, a significant decrease in the number of POMC-immunoreactive (POMC-ir) cells in the Arc in the two groups of females treated with genistein was observed. In contrast, no alteration in orexin expression was detected in any of the structures analyzed in either males or females. In conclusion, genistein can modulate estradiol’s programming actions on the hypothalamic feeding circuits differentially in male and female rats during development. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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21 pages, 4200 KiB

Open AccessArticle

Impact of Long-Term HFD Intake on the Peripheral and Central IGF System in Male and Female Mice

by Santiago Guerra-Cantera, Laura M. Frago, María Jiménez-Hernaiz, Purificación Ros, Alejandra Freire-Regatillo, Vicente Barrios, Jesús Argente and Julie A. Chowen

Metabolites 2020, 10(11), 462; https://doi.org/10.3390/metabo10110462 - 13 Nov 2020

Cited by 8 | Viewed by 3221

Abstract

The insulin-like growth factor (IGF) system is responsible for growth, but also affects metabolism and brain function throughout life. New IGF family members (i.e., pappalysins and stanniocalcins) control the availability/activity of IGFs and are implicated in growth. However, how diet and obesity modify this system has been poorly studied. We explored how intake of a high-fat diet (HFD) or commercial control diet (CCD) affects the IGF system in the circulation, visceral adipose tissue (VAT) and hypothalamus. Male and female C57/BL6J mice received HFD (60% fat, 5.1 kcal/g), CCD (10% fat, 3.7 kcal/g) or chow (3.1 % fat, 3.4 kcal/g) for 8 weeks. After 7 weeks of HFD intake, males had decreased glucose tolerance (p < 0.01) and at sacrifice increased plasma insulin (p < 0.05) and leptin (p < 0.01). Circulating free IGF1 (p < 0.001), total IGF1 (p < 0.001), IGF2 (p < 0.05) and IGFBP3 (p < 0.01) were higher after HFD in both sexes, with CCD increasing IGFBP2 in males (p < 0.001). In VAT, HFD reduced mRNA levels of IGF2 (p < 0.05), PAPP-A (p < 0.001) and stanniocalcin (STC)-1 (p < 0.001) in males. HFD increased hypothalamic IGF1 (p < 0.01), IGF2 (p < 0.05) and IGFBP5 (p < 0.01) mRNA levels, with these changes more apparent in females. Our results show that diet-induced changes in the IGF system are tissue-, sex- and diet-dependent. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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Review

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12 pages, 1480 KiB

Open AccessReview

Extrahypothalamic Control of Energy Balance and Its Connection with Reproduction: Roles of the Amygdala

by Rafael Pineda, Encarnacion Torres and Manuel Tena-Sempere

Metabolites 2021, 11(12), 837; https://doi.org/10.3390/metabo11120837 - 3 Dec 2021

Cited by 5 | Viewed by 2924

Abstract

Body energy and metabolic homeostasis are exquisitely controlled by multiple, often overlapping regulatory mechanisms, which permit the tight adjustment between fuel reserves, internal needs, and environmental (e.g., nutritional) conditions. As such, this function is sensitive to and closely connected with other relevant bodily systems, including reproduction and gonadal function. The aim of this mini-review article is to summarize the most salient experimental data supporting a role of the amygdala as a key brain region for emotional learning and behavior, including reward processing, in the physiological control of feeding and energy balance. In particular, a major focus will be placed on the putative interplay between reproductive signals and amygdala pathways, as it pertains to the control of metabolism, as complementary, extrahypothalamic circuit for the integral control of energy balance and gonadal function. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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16 pages, 1143 KiB

Open AccessReview

Astrocyte Gliotransmission in the Regulation of Systemic Metabolism

by Cahuê De Bernardis Murat and Cristina García-Cáceres

Metabolites 2021, 11(11), 732; https://doi.org/10.3390/metabo11110732 - 26 Oct 2021

Cited by 20 | Viewed by 4203

Abstract

Normal brain function highly relies on the appropriate functioning of astrocytes. These glial cells are strategically situated between blood vessels and neurons, provide significant substrate support to neuronal demand, and are sensitive to neuronal activity and energy-related molecules. Astrocytes respond to many metabolic conditions and regulate a wide array of physiological processes, including cerebral vascular remodeling, glucose sensing, feeding, and circadian rhythms for the control of systemic metabolism and behavior-related responses. This regulation ultimately elicits counterregulatory mechanisms in order to couple whole-body energy availability with brain function. Therefore, understanding the role of astrocyte crosstalk with neighboring cells via the release of molecules, e.g., gliotransmitters, into the parenchyma in response to metabolic and neuronal cues is of fundamental relevance to elucidate the distinct roles of these glial cells in the neuroendocrine control of metabolism. Here, we review the mechanisms underlying astrocyte-released gliotransmitters that have been reported to be crucial for maintaining homeostatic regulation of systemic metabolism. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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20 pages, 1164 KiB

Open AccessReview

l-Lactate: Food for Thoughts, Memory and Behavior

by María Fernanda Veloz Castillo, Pierre J. Magistretti and Corrado Calì

Metabolites 2021, 11(8), 548; https://doi.org/10.3390/metabo11080548 - 20 Aug 2021

Cited by 21 | Viewed by 4795

Abstract

More and more evidence shows how brain energy metabolism is the linkage between physiological and morphological synaptic plasticity and memory consolidation. Different types of memory are associated with differential inputs, each with specific inputs that are upstream diverse molecular cascades depending on the receptor activity. No matter how heterogeneous the response is, energy availability represents the lowest common denominator since all these mechanisms are energy consuming and the brain networks adapt their performance accordingly. Astrocytes exert a primary role in this sense by acting as an energy buffer; glycogen granules, a mechanism to store glucose, are redistributed at glance and conveyed to neurons via the Astrocyte–Neuron Lactate Shuttle (ANLS). Here, we review how different types of memory relate to the mechanisms of energy delivery in the brain. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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16 pages, 1116 KiB

Open AccessReview

Sensory Circumventricular Organs, Neuroendocrine Control, and Metabolic Regulation

by Jin Kwon Jeong, Samantha A. Dow and Colin N. Young

Metabolites 2021, 11(8), 494; https://doi.org/10.3390/metabo11080494 - 29 Jul 2021

Cited by 17 | Viewed by 5944

Abstract

The central nervous system is critical in metabolic regulation, and accumulating evidence points to a distributed network of brain regions involved in energy homeostasis. This is accomplished, in part, by integrating peripheral and central metabolic information and subsequently modulating neuroendocrine outputs through the paraventricular and supraoptic nucleus of the hypothalamus. However, these hypothalamic nuclei are generally protected by a blood-brain-barrier limiting their ability to directly sense circulating metabolic signals—pointing to possible involvement of upstream brain nuclei. In this regard, sensory circumventricular organs (CVOs), brain sites traditionally recognized in thirst/fluid and cardiovascular regulation, are emerging as potential sites through which circulating metabolic substances influence neuroendocrine control. The sensory CVOs, including the subfornical organ, organum vasculosum of the lamina terminalis, and area postrema, are located outside the blood-brain-barrier, possess cellular machinery to sense the metabolic interior milieu, and establish complex neural networks to hypothalamic neuroendocrine nuclei. Here, evidence for a potential role of sensory CVO-hypothalamic neuroendocrine networks in energy homeostasis is presented. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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27 pages, 2686 KiB

Open AccessReview

Control of Adipose Cell Browning and Its Therapeutic Potential

by Fernando Lizcano and Felipe Arroyave

Metabolites 2020, 10(11), 471; https://doi.org/10.3390/metabo10110471 - 19 Nov 2020

Cited by 20 | Viewed by 4606

Abstract

Adipose tissue is the largest endocrine organ in humans and has an important influence on many physiological processes throughout life. An increasing number of studies have described the different phenotypic characteristics of fat cells in adults. Perhaps one of the most important properties of fat cells is their ability to adapt to different environmental and nutritional conditions. Hypothalamic neural circuits receive peripheral signals from temperature, physical activity or nutrients and stimulate the metabolism of white fat cells. During this process, changes in lipid inclusion occur, and the number of mitochondria increases, giving these cells functional properties similar to those of brown fat cells. Recently, beige fat cells have been studied for their potential role in the regulation of obesity and insulin resistance. In this context, it is important to understand the embryonic origin of beige adipocytes, the response of adipocyte to environmental changes or modifications within the body and their ability to transdifferentiate to elucidate the roles of these cells for their potential use in therapeutic strategies for obesity and metabolic diseases. In this review, we discuss the origins of the different fat cells and the possible therapeutic properties of beige fat cells. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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10 pages, 874 KiB

Open AccessBrief Report

Evidence That Agouti-Related Peptide May Directly Regulate Kisspeptin Neurons in Male Sheep

by Christina M. Merkley, Sydney L. Shuping, Jeffrey R. Sommer and Casey C Nestor

Metabolites 2021, 11(3), 138; https://doi.org/10.3390/metabo11030138 - 26 Feb 2021

Cited by 12 | Viewed by 2522

Abstract

Agouti-related peptide (AgRP) neurons, which relay information from peripheral metabolic signals, may constitute a key central regulator of reproduction. Given that AgRP inhibits luteinizing hormone (LH) secretion and that nutritional suppression of LH elicits an increase in AgRP while suppressing kisspeptin expression in the arcuate nucleus (ARC) of the hypothalamus, we sought to examine the degree to which AgRP could directly regulate ARC kisspeptin neurons. Hypothalamic tissue was collected from four castrated male sheep (10 months of age) and processed for the detection of protein (AgRP input to kisspeptin neurons) using immunohistochemistry and mRNA for melanocortin 3 and 4 receptors (MC3R; MC4R) in kisspeptin neurons using RNAscope. Immunohistochemical analysis revealed that the majority of ARC kisspeptin neurons are contacted by presumptive AgRP terminals. RNAscope analysis revealed that nearly two thirds of the ARC kisspeptin neurons express mRNA for MC3R, while a small percentage (<10%) colocalize MC4R. Taken together, this data provides neuroanatomical evidence for a direct link between orexigenic AgRP neurons and reproductively critical kisspeptin neurons in the sheep, and builds upon our current understanding of the central link between energy balance and reproduction. Full article

(This article belongs to the Special Issue Neuroendocrine Control of Energy Metabolism)

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