Exercise increases NPY/AgRP and TH neuron activity in the hypothalamus of female mice

in Journal of Endocrinology
Authors:
Taylor Landry East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA

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Daniel Shookster East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA

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Alec Chaves East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA

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Katrina Free East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA

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Tony Nguyen East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA

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Hu Huang East Carolina Diabetes and Obesity Institute, East Carolina University, Greenville, North Carolina, USA
Department of Kinesiology, East Carolina University, Greenville, North Carolina, USA
Human Performance Laboratory, College of Human Performance and Health, East Carolina University, Greenville, North Carolina, USA
Department of Physiology, East Carolina University, Greenville, North Carolina, USA

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Correspondence should be addressed to H Huang: huangh@ecu.edu
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Recent evidence identifies a potent role for aerobic exercise to modulate the activity of hypothalamic neurons related to appetite; however, these studies have been primarily performed in male rodents. Since females have markedly different neuronal mechanisms regulating food intake, the current study aimed to determine the effects of acute treadmill exercise on hypothalamic neuron populations involved in regulating appetite in female mice. Mature, untrained female mice were exposed to acute sedentary, low- (10 m/min), moderate- (14 m/min), and high (18 m/min)-intensity treadmill exercise in a randomized crossover design. Mice were fasted 10 h before exercise, and food intake was monitored for 48 h after bouts. Immunohistochemical detection of cFOS was performed 3 h post-exercise to determine the changes in hypothalamic neuropeptide Y (NPY)/agouti-related peptide (AgRP), pro-opiomelanocortin (POMC), tyrosine hydroxylase (TH), and SIM1-expressing neuron activity concurrent with the changes in food intake. Additionally, stains for pSTAT3tyr705 and pERKthr202/tyr204 were performed to detect exercise-mediated changes in intracellular signaling. Briefly, moderate- and high-intensity exercises increased 24-h food intake by 5.9 and 19%, respectively, while low-intensity exercise had no effects. Furthermore, increases in NPY/AgRPARC, SIM1PVN, and TH neuron activity were observed 3 h after high-intensity exercise, with no effects on POMCARC neurons. While no effects of exercise on pERKthr202/tyr204 were observed, pSTAT3tyr705 was elevated specifically in NPY/AgRP neurons 3 h post-exercise. Overall, aerobic exercise increased the activity of several appetite-stimulating neuron populations in the hypothalamus of female mice, which may provide insight into previously reported sexual dimorphisms in post-exercise feeding.

 

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  • Alajmi N, Deighton K, King JA, Reischak-Oliviera A, Wasse LK, Jones J, Batterham RL & Stensel DJ 2016 Appetite and energy intake responses to acute energy deficits in females versus males. Medicine and Science in Sports and Exercise 48 412–420. (https://doi.org/10.1249/MSS.0000000000000793)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Applegate EA, Upton DE & Stern JS 1982 Food intake, body composition and blood lipids following treadmill exercise in male and female rats. Physiology and Behavior 28 917920. (https://doi.org/10.1016/0031-9384(8290214-1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ballor DL & Keesey RE 1991 A meta-analysis of the factors affecting exercise-induced changes in body mass, fat mass and fat-free mass in males and females. International Journal of Obesity 15 717726. (PMID: https://pubmed.ncbi.nlm.nih.gov/1838100/)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bobinski F, Teixeira JM, Sluka KA & Adair Santos ARS 2018 Interleukin-4 mediates the analgesia produced by low-intensity exercise in mice with neuropathic pain. Pain 159 437450. (https://doi.org/10.1097/j.pain.0000000000001109)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borghouts LB & Keizer HA 2000 Exercise and insulin sensitivity: a review. International Journal of Sports Medicine 21 112. (https://doi.org/10.1055/s-2000-8847)

  • Bouassida A, Zalleg D, Bouassida S, Zaouali M, Feki Y, Zbidi A & Tabka Z 2006 Leptin, its implication in physical exercise and training: a short review. Journal of Sports Science and Medicine 5 172181. (PMCID: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3827558/)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Brennan IM, Feltrin KL, Nair NS, Hausken T, Little TJ, Gentilcore D, Wishart JM, Jones KL, Horowitz M & Feinle-Bisset C 2009 Effects of the phases of the menstrual cycle on gastric emptying, glycemia, plasma GLP-1 and insulin, and energy intake in healthy lean women. American Journal of Physiology: Gastrointestinal and Liver Physiology 297 G602G610. (https://doi.org/10.1152/ajpgi.00051.2009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bunner W, Landry T, Laing BT, Li P, Rao Z, Yuan Y & Huang H 2020 ARCAgRP/NPY neuron activity is required for acute exercise-induced food intake in un-trained mice. Frontiers in Physiology 11 411. (https://doi.org/10.3389/fphys.2020.00411)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Calvez J, Fromentin G, Nadkarni N, Darcel N, Even P, Tomé D, Ballet N & Chaumontet C 2011 Inhibition of food intake induced by acute stress in rats is due to satiation effects. Physiology and Behavior 104 675683. (https://doi.org/10.1016/j.physbeh.2011.07.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen SR, Chen H, Zhou JJ, Pradhan G, Sun Y, Pan HL & Li DP 2017 Ghrelin receptors mediate ghrelin-induced excitation of agouti-related protein/neuropeptide Y but not pro-opiomelanocortin neurons. Journal of Neurochemistry 142 512520. (https://doi.org/10.1111/jnc.14080)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Church TS, Martin CK, Thompson AM, Earnest CP, Mikus CR & Blair SN 2009 Changes in weight, waist circumference and compensatory responses with different doses of exercise among sedentary, overweight postmenopausal women. PLoS ONE 4 e4515. (https://doi.org/10.1371/journal.pone.0004515)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Clegg DJ, Riedy CA, Smith KAB, Benoit SC & Woods SC 2003 Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 52 682687. (https://doi.org/10.2337/diabetes.52.3.682)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dorling J, Broom DR, Burns SF, Clayton DJ, Deighton K, James LJ, King JA, Miyashita M, Thackray AE & Batterham RL et al.2018 Acute and chronic effects of exercise on appetite, energy intake, and appetite-related hormones: the modulating effect of adiposity, sex, and habitual physical activity. Nutrients 10 1140. (https://doi.org/10.3390/nu10091140)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Douglas JA, King JA, McFarlane E, Baker L, Bradley C, Crouch N, Hill D & Stensel DJ 2015 Appetite, appetite hormone and energy intake responses to two consecutive days of aerobic exercise in healthy young men. Appetite 92 5765. (https://doi.org/10.1016/j.appet.2015.05.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Durrant ML, Royston JP & Wloch RT 1982 Effect of exercise on energy intake and eating patterns in lean and obese humans. Physiology and Behavior 29 449454. (https://doi.org/10.1016/0031-9384(8290265-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ebrahimi M, Rahmani-Nia F, Damirchi A, Mirzaie B & Pur SA 2013 Effect of short-term exercise on appetite, energy intake and energy-regulating hormones. Iranian Journal of Basic Medical Sciences 16 829834. (https://doi.org/10.22038/ijbms.2013.1117)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Goodin SZ, Keichler AR, Smith M, Wendt D & Strader AD 2008 Effect of gonadectomy on AgRP-induced weight gain in rats. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 295 R1747R1753. (https://doi.org/10.1152/ajpregu.90345.2008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hagobian TA, Yamashiro M, Hinkel-Lipsker J, Streder K, Evero N & Hackney T 2013 Effects of acute exercise on appetite hormones and ad libitum energy intake in men and women. Applied Physiology, Nutrition and Metabolism 38 6672. (https://doi.org/10.1139/apnm-2012-0104)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hallworth JR, Copeland JL, Doan J & Hazell TJ 2017 The effect of exercise intensity on total PYY and GLP-1 in healthy females: a pilot study. Journal of Nutrition and Metabolism 2017 4823102. (https://doi.org/10.1155/2017/4823102)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hazell TJ, Townsend LK, Hallworth JR, Doan J & Copeland JL 2017 Sex differences in the response of total PYY and GLP-1 to moderate-intensity continuous and sprint interval cyclinG exercise. European Journal of Applied Physiology 117 431440. (https://doi.org/10.1007/s00421-017-3547-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • He Z, Gao Y, Alhadeff AL, Castorena CM, Huang Y, Lieu L, Afrin S, Sun J, Betley JN & Guo H et al.2018 Cellular and synaptic reorganization of arcuate NPY/AgRP and POMC neurons after exercise. Molecular Metabolism 18 107119. (https://doi.org/10.1016/j.molmet.2018.08.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jackson M, Fatahi F, Alabduljader K, Jelleyman C, Moore JP & Kubis HP 2018 Exercise training and weight loss, not always a happy marriage: single blind exercise trials in females with diverse BMI. Applied Physiology, Nutrition and Metabolism 43 363370. (https://doi.org/10.1139/apnm-2017-0577)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Jeong JH, Lee DK, Liu SM, Chua SC, Schwartz GJ & Jo YH 2018 Activation of temperature-sensitive TRPV1-like receptors in ARC POMC neurons reduces food intake. PLoS Biology 16 e2004399. (https://doi.org/10.1371/journal.pbio.2004399)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kim YA, Pitriani P, Park HG & Lee WL 2019 Moderate intensity exercise has more positive effects on the gene expression of inflammasome, M1, M2 macrophage infiltration and brown adipocyte markers compared to high intensity exercise in subcutaneous adipose of obese mice induced by high fat diet. Journal of Life Science 29 303310. (https://doi.org/10.5352/JLS.2019.29.3.303)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • King NA, Snell L, Smith RD & Blundell JE 1996 Effects of short-term exercise on appetite responses in unrestrained females. European Journal of Clinical Nutrition 50 663667.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kissileff HR, Pi-Sunyer FX, Segal K, Meltzer S & Foelsch PA 1990 Acute effects of exercise on food intake in obese and nonobese women. American Journal of Clinical Nutrition 52 240245. (https://doi.org/10.1093/ajcn/52.2.240)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Krashes MJ, Koda S, Ye C, Rogan SC, Adams AC, Cusher DS, Maratos-Flier E, Roth BL & Lowell BB 2011 Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. Journal of Clinical Investigation 121 14241428. (https://doi.org/10.1172/JCI46229)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Krashes MJ, Shah BP, Madara JC, Olson DP, Strochlic DE, Garfield AS, Vong L, Pei H, Watabe-Uchida M & Uchida N et al.2014 An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 507 238242. (https://doi.org/10.1038/nature12956)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Landry T, Shookster D, Chaves A, Free K, Nguyen T & Huang H 2021a Energy status differentially modifies feeding behavior and POMCARC neuron activity after acute treadmill exercise in untrained mice. Frontiers in Endocrinology 12 705267. (https://doi.org/10.3389/fendo.2021.705267)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Landry T, Li P, Shookster D, Jiang Z, Li H, Laing BT, Bunner W, Langton T, Tong Q & Huang H 2021b Centrally circulating α-klotho inversely correlates with human obesity and modulates arcuate cell populations in mice. Molecular Metabolism 44 101136. (https://doi.org/10.1016/j.molmet.2020.101136)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Larson-Meyer DE, Palm S, Bansal A, Austin KJ, Hart AM & Alexander BM 2012 Influence of running and walking on hormonal regulators of appetite in women. Journal of Obesity 2012 730409. (https://doi.org/10.1155/2012/730409)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lieu L, Chau D, Afrin S, Dong Y, Alhadeff AL, Betley JN & Williams KW 2020 Effects of metabolic state on the regulation of melanocortin circuits. Physiology and Behavior 224 113039. (https://doi.org/10.1016/j.physbeh.2020.113039)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lin X, Itoga CA, Taha S, Li MH, Chen R, Sami K, Berton F, Francesconi W & Xu X 2018 C-Fos mapping of brain regions activated by multi-modal and electric foot shock stress. Neurobiology of Stress 8 92102. (https://doi.org/10.1016/j.ynstr.2018.02.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lissner L, Stevens J, Levitsky DA, Rasmussen KM & Strupp BJ 1988 Variation in energy intake during the menstrual cycle: implications for food-intake research. American Journal of Clinical Nutrition 48 956962. (https://doi.org/10.1093/ajcn/48.4.956)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mani BK, Castorena CM, Lawrence SO, Vijayaraghavan P, Metzger NP, Elmquist JK & Zigman JM 2018 Ghrelin mediates exercise endurance and the feeding response post-exercise. Molecular Metabolism 9 114130. (https://doi.org/10.1016/j.molmet.2018.01.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mayer CM & Belsham DD 2009 Insulin directly regulates NPY and AgRP gene expression via the MAPK MEK/ERK signal transduction pathway in MHypoE-46 hypothalamic neurons. Molecular and Cellular Endocrinology 307 99108. (https://doi.org/10.1016/j.mce.2009.02.031)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Melzer K, Kayser B, Waris WHM & Pichard C 2005 Effects of physical activity on food intake. Clinical Nutrition 24 885895. (https://doi.org/10.1016/j.clnu.2005.06.003)

  • Mesaros A, Koralov SB, Rother E, Wunderlich FT, Ernst MB, Barsh GS, Rajewsky K & Brüning JC 2008 Activation of Stat3 signaling in AgRP neurons promotes locomotor activity. Cell Metabolism 7 236248. (https://doi.org/10.1016/J.CMET.2008.01.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Miletta MC, Iyilikci O, Shanabrough M, Šestan-Peša M, Cammisa A, Zeiss CJ, Dietrich MO & Horvath TL 2020 AgRP neurons control compulsive exercise and survival in an activity-based anorexia model. Nature Metabolism 2 12041211. (https://doi.org/10.1038/s42255-020-00300-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Münzberg H, Jobst EE, Bates SH, Jones J, Villanueva E, Leshan R, Björnholm M, Elmquist J, Sleeman M & Cowley MA et al.2007 Appropriate inhibition of orexigenic hypothalamic arcuate nucleus neurons independently of leptin receptor/STAT3 signaling. Journal of Neuroscience 27 6974. (https://doi.org/10.1523/JNEUROSCI.3168-06.2007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nance DM, Bromley B, Barnard RJ & Gorski RA 1977 Sexually dimorphic effects of forced exercise on food intake and body weight in the rat. Physiology and Behavior 19 155158. (https://doi.org/10.1016/0031-9384(7790173-1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nohara K, Zhang Y, Waraich RS, Laque A, Tiano JP, Tong J, Münzberg H & Mauvais-Jarvis F 2011 Early-life exposure to testosterone programs the hypothalamic melanocortin system. Endocrinology 152 16611669. (https://doi.org/10.1210/en.2010-1288)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Oscai LB, Molé PA & Holloszy JO 1971 Effects of exercise on cardiac weight and mitochondria in male and female rats. American Journal of Physiology 220 19441948. (https://doi.org/10.1152/ajplegacy.1971.220.6.1944)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pomerleau M, Imbeault P, Parker T & Doucet E 2004 Effects of exercise intensity on food intake and appetite in women. American Journal of Clinical Nutrition 80 12301236. (https://doi.org/10.1093/ajcn/80.5.1230)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Qiu J, Zhang C, Borgquist A, Nestor CC, Smith AW, Bosch MA, Ku S, Wagner EJ, Rønnekleiv OK & Kelly MJ 2014 Insulin excites anorexigenic proopiomelanocortin neurons via activation of canonical transient receptor potential channels. Cell Metabolism 19 682693. (https://doi.org/10.1016/j.cmet.2014.03.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Qu N, He Y, Wang C, Xu P, Yang Y, Cai X, Liu H, Yu K, Pei Z & Hyseni I et al.2020 A POMC-originated circuit regulates stress-induced hypophagia, depression, and anhedonia. Molecular Psychiatry 25 10061021. (https://doi.org/10.1038/s41380-019-0506-1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rahmouni K, Sigmund CD, Haynes WG & Mark AL 2009 Hypothalamic ERK mediates the anorectic and thermogenic sympathetic effects of leptin. Diabetes 58 536542. (https://doi.org/10.2337/db08-0822)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ropelle ER, Flores MB, Cintra DE, Rocha GZ, Pauli JR, Morari J, de Souza CT, Moraes JC, Prada PO & Guadagnini D et al.2010 IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKβ and ER stress inhibition. PLoS Biology 8 3132. (https://doi.org/10.1371/journal.pbio.1000465)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shi YC, Lau J, Lin Z, Zhang H, Zhai L, Sperk G, Heilbronn R, Mietzsch M, Weger S & Huang XF et al.2013 Arcuate NPY controls sympathetic output and BAT function via a relay of tyrosine hydroxylase neurons in the PVN. Cell Metabolism 17 236248. (https://doi.org/10.1016/j.cmet.2013.01.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Skov LJ, Ratner C, Hansen NW, Thompson JJ, Egerod KL, Burm H, Dalbøge LS, Hedegaard MA, Brakebusch C & Pers TH et al.2019 RhoA in tyrosine hydroxylase neurones regulates food intake and body weight via altered sensitivity to peripheral hormones. Journal of Neuroendocrinology 31 e12761. (https://doi.org/10.1111/jne.12761)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Staten MA 1991 The effect of exercise on food intake in men and women. American Journal of Clinical Nutrition 53 2731. (https://doi.org/10.1093/ajcn/53.1.27)

  • Thackray AE, Deighton K, King JA & Stensel DJ 2016 Exercise, appetite and weight control: are there differences between men and women? Nutrients 8 583. (https://doi.org/10.3390/nu8090583)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tong Q, Ye CP, Jones JE, Elmquist JK & Lowell BB 2008 Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nature Neuroscience 11 9981000. (https://doi.org/10.1038/nn.2167)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Unick JL, Otto AD, Goodpaster BH, Helsel DL, Pellegrini CA & Jakicic JM 2010 Acute effect of walking on energy intake in overweight/obese women. Appetite 55 413419. (https://doi.org/10.1016/J.APPET.2010.07.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Urban JH, Bauer-Dantoin AC & Levine JE 1993 Neuropeptide Y gene expression in the arcuate nucleus: sexual dimorphism and modulation by testosterone. Endocrinology 132 139145. (https://doi.org/10.1210/endo.132.1.8419120)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Varela L & Horvath TL 2012 Leptin and insulin pathways in POMC and AgRP neurons that modulate energy balance and glucose homeostasis. EMBO Reports 13 10791086. (https://doi.org/10.1038/embor.2012.174)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Walker QD, Rooney MB, Wightman RM & Kuhn CM 2000 Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 95 10611070. (https://doi.org/10.1016/S0306-4522(9900500-X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xu Y, Nedungadi TP, Zhu L, Sobhani N, Irani BG, Davis KE, Zhang X, Zou F, Gent LM & Hahner LD et al.2011 Distinct hypothalamic neurons mediate estrogenic effects on energy homeostasis and reproduction. Cell Metabolism 14 453465. (https://doi.org/10.1016/j.cmet.2011.08.009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhan C, Zhou J, Feng Q, Zhang JE, Lin S, Bao J, Wu P & Luo M 2013 Acute and long-term suppression of feeding behavior by POMC neurons in the brainstem and hypothalamus, respectively. Journal of Neuroscience 33 36243632. (https://doi.org/10.1523/JNEUROSCI.2742-12.2013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang X & van den Pol AN 2016 Hypothalamic arcuate nucleus tyrosine hydroxylase neurons play orexigenic role in energy homeostasis. Nature Neuroscience 19 13411347. (https://doi.org/10.1038/nn.4372)

    • PubMed
    • Search Google Scholar
    • Export Citation