Reactive oxygen species signaling influences feeding behaviour
DOI:
https://doi.org/10.18203/2320-6012.ijrms20151135Keywords:
Agouti related peptide (AgRP), Feeding behaviour, Neuro-peptide Y (NPY) neurons, Pro-opiomelanocortin (POMC) neurons, Reactive oxygen species (ROS)Abstract
Reactive Oxygen Species (ROS) are not just by products of substrate oxidation but also chemicals that are involved in intracellular signaling when they are generated transiently and moderately. This review explores the intracellular signaling aspects of reactive oxygen species in influencing feeding behaviour. Substrates like glucose and lipids stimulate generation of reactive oxygen species mainly through mitochondria and to some extent through the NADPH oxidases. The level of ROS generated in hypothalamic neurons like NPY/AgRP and POMC neurons, under the influence of substrate level, directly influences the activity of these neurons and subsequently affect the downstream neurons located in other parts of the hypothalamus like the ventromedial nucleus (VMN), the paraventricular nucleus (PVN) and the lateral hypothalamus. Activation of POMC neuronal population is driven by increase ROS level whereas activation of NPY/AgRP neurons occurs when ROS level is reduced. The activation of these neurons will determine the feeding behaviour which will either be satiety if POMC neurons are activated or increase food intake if NPY/AgRP neurons are activated.
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Bashan N, Kovsan J, Kachko I, Ovadia H, Rudich A. Positive and negative regulation of insulin signaling by reactive oxygen and nitrogen species. Physiol Rev. 2009;89:27-71.
Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol. 2004;4:181-9.
Peterson OH, Spat A, Verkhratsy A. Introduction: reactive oxygen species in health and disease. Phil Trans R Soc B. 2005;360:2197-9.
Cross AR, Jones OT. Enzymic mechanisms of superoxide production. Biochem Biophys Acta. 1991;1057:281-98.
Schrader M, Fahimi HD. Peroxisomes and oxidative stress. Biochim Biophys Acta. 2006;1763:1755-66.
Tretter L, Adam-Vizi V. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Phil Trans R Soc. 2005;B360:2335-45.
Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47-95.
Clark SF. The biochemistry of antioxidants revisited. Nutr Clin Pract. 2002;17:5-17.
Infanger DW, Sharma RV, Davission RL. NADPH oxidases of the brain: distribution, regulation, and function. Antioxid Redox Signal. 2006;8:1583-96.
Drougard A, Fournel A, Valet P, Knauf C. Impact of hypothalamic reactive oxygen species in the regulation of energy metabolism and food intake. Frontiers Neurosci. 2015;9:56.
Leloup C, Magnan C, Benani A, Bonnet E, Alquier T, Offer G, et al. Mitochondrial reactive oxygen species are required for hypothalamic glucose sensing. Diabetes. 2006;55:2084-90.
Andrews ZB, Liu ZW, Wallingford N, Erison DM, Borok E, Friedman JM, et al. UCP2 mediates ghrelin’s action on NPY/AgRP neurons by lowering free radicals. Nature. 2008;454:846-51.
Ibrahim N, Bosch MA, Smart JL, Qiu J, Rubinstein, M, Ronnekleiv OK, et al. Hypothalamic proopio melanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology. 2003;144:1331-40.
Mountjoy PD, Bailey SJ, Rutter GA. Inhibition by glucose or leptin of hypothalamic neurons expressing neuropeptide Y requires changes in AMP-activated protein kinase activity. Diabetologia. 2007;50:168-77.
Kuo DY, Chen PN, Yang SF, Chu SC, Chen CH, Kuo MH, et al. Role of reactive oxygen species-related enzymes in neuropeptide y and pro-opio melanocortin mediated appetite control: a study using atypical protein kinase C knockdown. Antioxid Redox Signal. 2011;15:2147-59.
Horvath TL, Andrews ZB, Diano S. Fuel utilization by hypothalamic neurons: roles for ROS. Trends Endocrinol Metab. 2009;20:78-87.
Diano S, Liu ZW, Jeong JK, Dietrich MO, Ruan HB, Kim E, et al. Peroxisome proliferation-associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat Med. 2011;17:1121-7.
Jaillard T, Roger M, Galinier A, Guillou P, Benani A, Leloup C, et al. Hypothalamic reactive oxygen species are required for insulin- induced food intake inhibition: an NADPH oxidase-dependent mechanism. Diabetes. 2009;58:1544-9.
Dietrich MO, Liu ZW, Horvath TL. Mitochondrial dynamics controlled by mitofusins regulate Agrp neuronal activity and diet-induced obesity. Cell. 2013;155:188-99.
Yoon Y, Galloway CA, Jhun BS, Yu T. Mitochondrial dynamics in diabetes. Antioxid Redox Signal. 2011;14:439-57.
Carneiro L, Allard C, Guissard C, Fioramonti X, Tourrel-Cuzin C, Bailbe D, et al. Importance of mitochondrial dynamin-related protein1 in hypothalamic glucose sensitivity in rats. Antioxid Redox Signal. 2012;17:433-44.
Aquila H, Link TA, Klingenberg M. The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane. EMBO J. 1985;4:2369-76.
Vozza A, Parisi G, DeLeonardis F, Lasorsa FM, Castegna A, Amorese D, et al. UCP2 transports C4 metabolites out of mitochondria, regulating glucose and glutamine oxidation. Proc Natl Acad Sci U.S.A. 2014;111:960-5.
Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, Portero-Otin M, et al. A signaling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO J. 2003;22:4103-10.
Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, et al. Mitochondrial superoxides: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med. 2004;37(6):755-67.
Coppola A, Liu ZW, Andrews ZB, Paradis E, Roy MC, Friedman JM, et al. A central thermogenic-like mechanism in feeding regulation: an interplay between arcuate nucleus T3 and UCP2. Cell Metab. 2007;5:21-33.
Hernandez-Fonseca K, Cardenas-Rodriguez N, Pedraza-Chaverri J, Massieu L. Calcium-dependent production of reactive oxygen species is involved in neuronal damage induced during glycolysis inhibition in cultured hippocampal neurons. J Neurosci Res. 2008;86:1768-80.
Kohno D, Sone H, Minokoshi Y, Yada T. Ghrelin raises [Ca 2+] i Via AMPK in hypothalamic arcuate nucleus NPY neurons. Biochem Biophys Res Communic. 2008;366:388-92.
Yang Y, Atasoy D, Su HH, Sternson SM. Hunger states switch a flip-flop memory circuit via a synaptic AMPK- dependent positive feedback loop. Cell. 2011;146(6):992-1003.
Cummings DE, Overduin J, Shannon MH, Foster Schubert KE. Hormonal mechanisms of weight loss and diabetes resolution after bariatric surgery. Surg Obes Relat Dis. 2005;1(3):358-68.
Oakhill JS, Steel R, Chen ZP, Scott JW, Ling N, Tam S, et al. AMPK is a direct adenylate charge-regulated protein kinase. Science. 2011;332(6036):1433-5.
Carling D. The role of AMP-activated protein kinase in the regulation of energy homeostasis. Novartis Found Symp. 2007;286:72-81, Discussion 81-75, 162, 196-203.
Weber AM, Wong FK, Tufford AR, Schlichter LC, Matveev V, Stanley EF. N-type Ca2+ channels carry the largest current: implications for nano domain sand transmitter release. Nat Neurosci. 2010;13:1348-50.
Gyengesi E, Paxinos G, Andrews ZB. Oxidative stress in the hypothalamus: the importance of calcium signaling and mitochondrial ROS in body weight regulation. Curr Neuropharmacol. 2012;10:344-53.
Berridge MJ. Calcium signaling remodeling and disease. Biochem Soc Trans. 2012;40:297-309.
Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, Gantz I, et al. Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science. 1997;278:135-8.
Belgardt BF, Okamura T, Bruning JC. Hormone and glucose signaling in POMC and AgRP neurons. J Physiol. 2009;587(22):5305-14.
Nishihara M, Hirooka Y, Matsukawa R, Kishi T, Sunagawa K. Oxidative stress in the rostral ventrolateral medulla modulates excitatory and inhibitory inputs in spontaneously hypertensive rats. J Hypertens. 2012;30(1):97-106.
Hirooka Y, Kishi T, Sakai K, Takeshita A, Sunagawa K. Imbalance of central nitric oxide and reactive oxygen species in the regulation of sympathetic activity and neural mechanisms of hypertension. Am J Physiol Regul Integr Comp Physiol. 2011;300:R818-26.
Campese VM, Shaohua Y, Huiquin Z. Oxidative stress mediates angiotensin II-dependent stimulation of sympathetic nerve activity. Hypertension. 2005;46:533-9.
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