Arcuate Na+,K+-ATPase senses systemic energy states and regulates feeding behavior through glucose-inhibited neurons

American Journal of Physiology - Endocrinology and Metabolism

Volumn 309, Issue 4, 2015, Pages E320-E333

  Kurita, Hideharu ^a   Xu, Kai Y ^b   Maejima, Yuko ^a   Nakata, Masanori ^a   Dezaki, Katsuya ^a   Santoso, Putra ^a   Yang, Yifei ^a   Arai, Takeshi ^a   Gantulga, Darambazar ^a   Muroya, Shinji ^c   Lefor, Alan K ^a   Kakei, Masafumi ^a   Watanabe, Eiju ^a   Yada, Toshihiko ^a,d  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c Imamura Bun in Hospital   (Japan)

^d NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Agouti related protein; Arcuate nucleus; ATP; Fasting; Feeding behavior; Ghrelin; Glucose; Glucose inhibited neuron; K+ ATPase; Na+; Neuropeptide Y; Ouabain; SSA412; 3 isoform

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AGOUTI RELATED PROTEIN; CALCIUM; GHRELIN; GLUCOSE; NEUROPEPTIDE Y; OUABAIN; PROOPIOMELANOCORTIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SHORT HAIRPIN RNA; ADENOSINE TRIPHOSPHATE; ATP1A3 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; CONCENTRATION PROCESS; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEEDING BEHAVIOR; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HYPOTHALAMUS; MALE; MOUSE; NERVE CELL; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; ENERGY METABOLISM; GENETICS; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; TRANSGENIC RAT;

ADENOSINE TRIPHOSPHATE; AGOUTI-RELATED PROTEIN; ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; BEHAVIOR, ANIMAL; ENERGY METABOLISM; FEEDING BEHAVIOR; GLUCOSE; MALE; NEURONS; NEUROPEPTIDE Y; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84939434790     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00446.2014     Document Type: Article

References (44)

1. + channels. J Physiol 544: 429–445, 2002.
2. Andrews ZB. Central mechanisms involved in the orexigenic actions of ghrelin. Peptides 32: 2248–2255, 2011.
3. Antonelli MC, Costa Lieste M, Baskin DG, Stahl WL, Schwartz MW. Localization of Na, K-ATPase isoforms in the hypothalamus of the rat. Cell Mol Biol (Noisy-le-grand) 41: 79–85, 1995.
4. Aponte Y, Atasoy D, Sternson SM. AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat Neurosci 14: 351–355, 2011.
5. Atasoy D, Betley JN, Su HH, Sternson SM. Deconstruction of a neural circuit for hunger. Nature 488: 172–177, 2012.
6. Baver SB, Hope K, Guyot S, Bjorbaek C, Kaczorowski C, O’Connell KM. Leptin modulates the intrinsic excitability of AgRP/NPY neurons in the arcuate nucleus of the hypothalamus. J Neurosci 34: 5486–5496, 2014.
7. Belgardt BF, Okamura T, Bruning JC. Hormone and glucose signaling in POMC and AgRP neurons. J Physiol 587: 5305–5314, 2009.
8. Blanco G, Mercer RW. Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol Renal Physiol 275: F633–F650, 1998.
9. Borg WP, Sherwin RS, During MJ, Borg MA, Shulman GI. Local ventromedial hypothalamus glucopenia triggers counterregulatory hormone release. Diabetes 44: 180–184, 1995.
10. Cone RD. Anatomy and regulation of the central melanocortin system. Nat Neurosci 8: 571–578, 2005.
11. Cowley MA, Smart JL, Rubinstein M, Cerdan MG, Diano S, Horvath TL, Cone RD, Low MJ. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411: 480–484, 2001.
12. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50: 1714–1719, 2001.
13. Darambazar G, Nakata M, Okada T, Wang L, Li E, Shinozaki A, Motoshima M, Mori M, Yada T. Paraventricular NUCB2/nesfatin-1 is directly targeted by leptin and mediates its anorexigenic effect. Biochem Biophys Res Commun 456: 913–918, 2015.
14. Dezaki K, Sone H, Koizumi M, Nakata M, Kakei M, Nagai H, Hosoda H, Kangawa K, Yada T. Blockade of pancreatic islet-derived ghrelin enhances insulin secretion to prevent high-fat diet-induced glucose intolerance. Diabetes 55: 3486–3493, 2006.
15. Eto K, Tsubamoto Y, Terauchi Y, Sugiyama T, Kishimoto T, Takahashi N, Yamauchi N, Kubota N, Murayama S, Aizawa T, Akanuma Y, Aizawa S, Kasai H, Yazaki Y, Kadowaki T. Role of NADH shuttle system in glucose-induced activation of mitochondrial metabolism and insulin secretion. Science 283: 981–985, 1999.
16. Gilon P, Henquin JC. Activation of muscarinic receptors increases the concentration of free Na+ in mouse pancreatic B-cells. FEBS Lett 315: 353–356, 1993.
17. Gropp E, Shanabrough M, Borok E, Xu AW, Janoschek R, Buch T, Plum L, Balthasar N, Hampel B, Waisman A, Barsh GS, Horvath TL, Bruning JC. Agouti-related peptide-expressing neurons are mandatory for feeding. Nat Neurosci 8: 1289–1291, 2005.
18. Kohno D, Gao HZ, Muroya S, Kikuyama S, Yada T. Ghrelin directly interacts with neuropeptide-Y-containing neurons in the rat arcuate nucleus: Ca2+ signaling via protein kinase A and N-type channel-dependent mechanisms and crosstalk with leptin and orexin. Diabetes 52: 948–956, 2003.
19. Kushner RF. Anti-obesity drugs. Expert Opin Pharmacother 9: 1339–1350, 2008.
20. +)-adenosine triphosphatase. J Biol Chem 247: 7634–7641, 1972.
21. Lam TK, Schwartz GJ, Rossetti L. Hypothalamic sensing of fatty acids. Nat Neurosci 8: 579–584, 2005.
22. Liu T, Kong D, Shah BP, Ye C, Koda S, Saunders A, Ding JB, Yang Z, Sabatini BL, Lowell BB. Fasting activation of AgRP neurons requires NMDA receptors and involves spinogenesis and increased excitatory tone. Neuron 73: 511–522, 2012.
23. Loftus TM, Jaworsky DE, Frehywot GL, Townsend CA, Ronnett GV, Lane MD, Kuhajda FP. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288: 2379–2381, 2000.
24. Luquet S, Perez FA, Hnasko TS, Palmiter RD. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310: 683–685, 2005.
25. Maejima Y, Sedbazar U, Suyama S, Kohno D, Onaka T, Takano E, Yoshida N, Koike M, Uchiyama Y, Fujiwara K, Yashiro T, Horvath TL, Dietrich MO, Tanaka S, Dezaki K, Oh IS, Hashimoto K, Shimizu H, Nakata M, Mori M, Yada T. Nesfatin-1-regulated oxytocinergic signaling in the paraventricular nucleus causes anorexia through a leptinindependent melanocortin pathway. Cell Metab 10: 355–365, 2009.
26. McMinn JE, Baskin DG, Schwartz MW. Neuroendocrine mechanisms regulating food intake and body weight. Obes Rev 1: 37–46, 2000.
27. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferre P, Birnbaum MJ, Stuck BJ, Kahn BB. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428: 569–574, 2004.
28. Muroya S, Yada T, Shioda S, Takigawa M. Glucose-sensitive neurons in the rat arcuate nucleus contain neuropeptide Y. Neurosci Lett 264: 113–116, 1999.
29. Oomura Y, Ono T, Ooyama H, Wayner MJ. Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222: 282–284, 1969.
30. Oomura Y, Ooyama H, Sugimori M, Nakamura T, Yamada Y. Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature 247: 284–286, 1974.
31. Oomura Y, Yoshimatsu H. Neural network of glucose monitoring system. J Auton Nerv Syst 10: 359–372, 1984.
32. Sainsbury A, Zhang L. Role of the arcuate nucleus of the hypothalamus in regulation of body weight during energy deficit. Mol Cell Endocrinol 316: 109–119, 2010.
33. Sakata I, Park WM, Walker AK, Piper PK, Chuang JC, Osborne-Lawrence S, Zigman JM. Glucose-mediated control of ghrelin release from primary cultures of gastric mucosal cells. Am J Physiol Endocrinol Metab 302: E1300–E1310, 2012.
34. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661–671, 2000.
35. Silver IA, Erecinska M. Glucose-induced intracellular ion changes in sugar-sensitive hypothalamic neurons. J Neurophysiol 79: 1733–1745, 1998.
36. Song Z, Levin BE, McArdle JJ, Bakhos N, Routh VH. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50: 2673–2681, 2001.
37. Spanswick D, Smith MA, Groppi VE, Logan SD, Ashford ML. Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature 390: 521–525, 1997.
38. Swanson LW, Ed. Brain Maps III: Structure of the Rat Brain. London, UK: Elsevier Academic, 2004.
39. Sweadner KJ, Goldin SM. Active transport of sodium and potassium ions: mechanism, function, and regulation. N Engl J Med 302: 777–783, 1980.
40. Tanaka S, Kurosumi K. A certain step of proteolytic processing of proopiomelanocortin occurs during the transition between two distinct stages of secretory granule maturation in rat anterior pituitary corticotrophs. Endocrinology 131: 779–786, 1992.
41. Willesen MG, Kristensen P, Romer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70: 306–316, 1999.
42. +)-ATPase. Biochem Biophys Res Commun 338: 1669–1677, 2005.
43. 2+]i-reducing action of cAMP in rat pancreatic β-cells: involvement of thapsigargin-sensitive stores. Am J Physiol Cell Physiol 274: C513–C521, 1998.
44. 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 146: 992–1003, 2011.