Glucose sensing mechanisms in hypothalamic cell models: Glucose inhibition of AgRP synthesis and secretion

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 262-270

  Chalmers, Jennifer A ^a   Jang, Janet J ^a   Belsham, Denise D ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Agouti related peptide; AMPK; Glucose; Hypothalamus; Neuropeptide

Indexed keywords

ADENYLATE KINASE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEOXYGLUCOSE; G PROTEIN COUPLED RECEPTOR; GLUCOSE; GLUCOSE TRANSPORTER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; NEUROPEPTIDE; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME IMMUNOASSAY; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HYPOTHALAMUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSOR; TASTE BUD;

AGOUTI-RELATED PEPTIDE; AMPK; GLUCOSE; HYPOTHALAMUS; NEUROPEPTIDE;

ADENYLATE KINASE; AGOUTI-RELATED PROTEIN; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE KINASE; CARNITINE O-PALMITOYLTRANSFERASE; CELL LINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DEOXYGLUCOSE; DOWN-REGULATION; GEMFIBROZIL; GLUCOSE; GREEN FLUORESCENT PROTEINS; HYPOTHALAMUS; MICE; MODELS, BIOLOGICAL; NEURONS; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE TYPE I; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PYRUVIC ACID; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER;

EID: 84886820170     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.10.013     Document Type: Article

References (53)

1. Anand B.K., Chhina G.S., Sharma K.N., Dua S., Singh B. Activity of single neurons in the hypothalamic feeding centers: effect of glucose. Am. J. Physiol. 1964, 207:1146-1154.
2. Bady I., Marty N., Dallaporta M., Emery M., Gyger J., Tarussio D., Foretz M., Thorens B. Evidence from glut2-null mice that glucose is a critical physiological regulator of feeding. Diabetes 2006, 55:988-995.
3. Beall C., Hamilton D.L., Gallagher J., Logie L., Wright K., Soutar M.P., Dadak S., Ashford F.B., Haythorne E., Du Q., Jovanovic A., Mccrimmon R.J., Ashford M.L. Mouse hypothalamic GT1-7 cells demonstrate AMPK-dependent intrinsic glucose-sensing behaviour. Diabetologia 2012, 55:2432-2444.
4. Belsham D.D., Cai F., Cui H., Smukler S.R., Salapatek A.M., Shkreta L. Generation of a phenotypic array of hypothalamic neuronal cell models to study complex neuroendocrine disorders. Endocrinology 2004, 145:393-400.
5. Belsham D.D., Fick L.J., Dalvi P.S., Centeno M.L., Chalmers J.A., Lee P.K., Wang Y., Drucker D.J., Koletar M.M. Ciliary neurotrophic factor recruitment of glucagon-like peptide-1 mediates neurogenesis, allowing immortalization of adult murine hypothalamic neurons. FASEB J. 2009, 23:4256-4265.
6. Cansell C., Denis R.G., Joly-Amado A., Castel J., Luquet S. Arcuate AgRP neurons and the regulation of energy balance. Front. Endocrinol. (Lausanne) 2012, 3:169.
7. Cha S.H., Wolfgang M., Tokutake Y., Chohnan S., Lane M.D. Differential effects of central fructose and glucose on hypothalamic malonyl-CoA and food intake. Proc. Natl. Acad. Sci. USA 2008, 105:16871-16875.
8. Cheng H., Isoda F., Belsham D.D., Mobbs C.V. Inhibition of agouti-related peptide expression by glucose in a clonal hypothalamic neuronal cell line is mediated by glycolysis, not oxidative phosphorylation. Endocrinology 2008, 149:703-710.
9. Chiang H.T., Cheng W.H., Lu P.J., Huang H.N., Lo W.C., Tseng Y.C., Wang J.L., Hsiao M., Tseng C.J. Neuronal nitric oxide synthase activation is involved in insulin-mediated cardiovascular effects in the nucleus tractus solitarii of rats. Neuroscience 2009, 159:727-734.
10. Clodfelder-Miller B., De Sarno P., Zmijewska A.A., Song L., Jope R.S. Physiological and pathological changes in glucose regulate brain Akt and glycogen synthase kinase-3. J. Biol. Chem. 2005, 280:39723-39731.
11. Creemers J.W., Pritchard L.E., Gyte A., Le Rouzic P., Meulemans S., Wardlaw S.L., Zhu X., Steiner D.F., Davies N., Armstrong D., Lawrence C.B., Luckman S.M., Schmitz C.A., Davies R.A., Brennand J.C., White A. Agouti-related protein is posttranslationally cleaved by proprotein convertase 1 to generate agouti-related protein (AGRP)83-132: interaction between AGRP83-132 and melanocortin receptors cannot be influenced by syndecan-3. Endocrinology 2006, 147:1621-1631.
12. Dalvi P.S., Nazarians-Armavil A., Tung S., Belsham D.D. Immortalized neurons for the study of hypothalamic function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R1030-R1052.
13. De Vries M.G., Arseneau L.M., Lawson M.E., Beverly J.L. Extracellular glucose in rat ventromedial hypothalamus during acute and recurrent hypoglycemia. Diabetes 2003, 52:2767-2773.
14. Dhillon S.S., Mcfadden S.A., Chalmers J.A., Centeno M.L., Kim G.L., Belsham D.D. Cellular leptin resistance impairs the leptin-mediated suppression of neuropeptide Y secretion in hypothalamic neurons. Endocrinology 2011, 152:4138-4147.
15. Donato J., Frazao R., Fukuda M., Vianna C.R., Elias C.F. Leptin induces phosphorylation of neuronal nitric oxide synthase in defined hypothalamic neurons. Endocrinology 2010, 151:5415-5427.
16. Dong Y.J., Chao A.C., Kouyama K., Hsu Y.P., Bocian R.C., Moss R.B., Gardner P. Activation of CFTR chloride current by nitric oxide in human T lymphocytes. EMBO J. 1995, 14:2700-2707.
17. Dunn-Meynell A.A., Rawson N.E., Levin B.E. Distribution and phenotype of neurons containing the ATP-sensitive K+ channel in rat brain. Brain Res. 1998, 814:41-54.
18. El-Husseini A.E., Williams J., Reiner P.B., Pelech S., Vincent S.R. Localization of the cGMP-dependent protein kinases in relation to nitric oxide synthase in the brain. J. Chem. Neuroanatomy 1999, 17:45-55.
19. Fioramonti X., Contie S., Song Z., Routh V.H., Lorsignol A., Penicaud L. Characterization of glucosensing neuron subpopulations in the arcuate nucleus: integration in neuropeptide Y and pro-opio melanocortin networks?. Diabetes 2007, 56:1219-1227.
20. Gadsby D.C., Nairn A.C. Control of CFTR channel gating by phosphorylation and nucleotide hydrolysis. Physiol. Rev. 1999, 79:S77-S107.
21. Garcia M.A., Carrasco M., Godoy A., Reinicke K., Montecinos V.P., Aguayo L.G., Tapia J.C., Vera J.C., Nualart F. Elevated expression of glucose transporter-1 in hypothalamic ependymal cells not involved in the formation of the brain-cerebrospinal fluid barrier. J. Cell Biochem. 2001, 80:491-503.
22. Gonzalez J.A., Jensen L.T., Fugger L., Burdakov D. Metabolism-independent sugar sensing in central orexin neurons. Diabetes 2008, 57:2569-2576.
23. Hallows K.R., Raghuram V., Kemp B.E., Witters L.A., Foskett J.K. Inhibition of cystic fibrosis transmembrane conductance regulator by novel interaction with the metabolic sensor AMP-activated protein kinase. J. Clin. Invest. 2000, 105:1711-1721.
24. Ibrahim N., Bosch M.A., Smart J.L., Qiu J., Rubinstein M., Ronnekleiv O.K., Low M.J., Kelly M.J. Hypothalamic proopiomelanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology 2003, 144:1331-1340.
25. Jahng J.W., Lee J.Y., Yoo S.B., Kim Y.M., Ryu V., Kang D.W., Lee J.H. Refeeding-induced expression of neuronal nitric oxide synthase in the rat paraventricular nucleus. Brain Res. 2005, 1048:185-192.
26. Joly-Amado A., Denis R.G., Castel J., Lacombe A., Cansell C., Rouch C., Kassis N., Dairou J., Cani P.D., Ventura-Clapier R., Prola A., Flamment M., Foufelle F., Magnan C., Luquet S. Hypothalamic AgRP-neurons control peripheral substrate utilization and nutrient partitioning. EMBO J. 2012, 31:4276-4288.
27. Kang L., Routh V.H., Kuzhikandathil E.V., Gaspers L.D., Levin B.E. Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 2004, 53:549-559.
28. Kawashima J., Alquier T., Tsuji Y., Peroni O.D., Kahn B.B. Ca2+/calmodulin-dependent protein kinase kinase is not involved in hypothalamic AMP-activated protein kinase activation by neuroglucopenia. PloS One 2012, 7:e36335.
29. Le Bacquer O., Queniat G., Gmyr V., Kerr-Conte J., Lefebvre B., Pattou F. MTORC1 and mTORC2 regulate insulin secretion through Akt in INS-1 cells. J. Endocrinol. 2013, 216:21-29.
30. Lee K., Li B., Xi X., Suh Y., Martin R.J. Role of neuronal energy status in the regulation of adenosine 5'-monophosphate-activated protein kinase, orexigenic neuropeptides expression, and feeding behavior. Endocrinology 2005, 146:3-10.
31. Lee Y.S., Sasaki T., Kobayashi M., Kikuchi O., Kim H.J., Yokota-Hashimoto H., Shimpuku M., Susanti V.Y., Ido-Kitamura Y., Kimura K., Inoue H., Tanaka-Okamoto M., Ishizaki H., Miyoshi J., Ohya S., Tanaka Y., Kitajima S., Kitamura T. Hypothalamic ATF3 is involved in regulating glucose and energy metabolism in mice. Diabetologia 2013, 56:1383-1393.
32. Levin B.E. Nutrient Sensing: Carbohydrates. Encyclopedia of Neuroscience 2009, 1295-1302.
33. Levin B.E., Routh V.H., Kang L., Sanders N.M., Dunn-Meynell A.A. Neuronal glucosensing: what do we know after 50 years?. Diabetes 2004, 53:2521-2528.
34. Li B., Xi X., Roane D.S., Ryan D.H., Martin R.J. Distribution of glucokinase, glucose transporter GLUT2, sulfonylurea receptor-1, glucagon-like peptide-1 receptor and neuropeptide Y messenger RNAs in rat brain by quantitative real time RT-PCR. Brain Res. Mol. Brain Res. 2003, 113:139-142.
35. Luquet S., Perez F.A., Hnasko T.S., Palmiter R.D. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 2005, 310:683-685.
36. Markert T., Vaandrager A.B., Gambaryan S., Pohler D., Hausler C., Walter U., De Jonge H.R., Jarchau T., Lohmann S.M. Endogenous expression of type II cGMP-dependent protein kinase mRNA and protein in rat intestine. Implications for cystic fibrosis transmembrane conductance regulator. J. Clin. Invest. 1995, 96:822-830.
37. Marty N., Dallaporta M., Thorens B. Brain glucose sensing, counterregulation, and energy homeostasis. Physiology 2007, 22:241-251.
38. Mobbs C.V., Kow L.M., Yang X.J. Brain glucose-sensing mechanisms: ubiquitous silencing by aglycemia vs. hypothalamic neuroendocrine responses. Am. J. Physiol. Endocrinol. Metab. 2001, 281:E649-E654.
39. Mountjoy P.D., Bailey S.J., Rutter G.A. Inhibition by glucose or leptin of hypothalamic neurons expressing neuropeptide Y requires changes in AMP-activated protein kinase activity. Diabetologia 2007, 50:168-177.
40. Murphy B.A., Fakira K.A., Song Z., Beuve A., Routh V.H. AMP-activated protein kinase and nitric oxide regulate the glucose sensitivity of ventromedial hypothalamic glucose-inhibited neurons. Am. J. Physiol. Cell Physiol. 2009, 297:C750-C758.
41. Murphy B.A., Fioramonti X., Jochnowitz N., Fakira K., Gagen K., Contie S., Lorsignol A., Penicaud L., Martin W.J., Routh V.H. Fasting enhances the response of arcuate neuropeptide Y-glucose-inhibited neurons to decreased extracellular glucose. Am. J. Physiol. Cell Physiol. 2009, 296:C746-C756.
42. Oomura Y., Ooyama H., Sugimori M., Nakamura T., Yamada Y. Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature 1974, 247:284-286.
43. Ren X., Zhou L., Terwilliger R., Newton S.S., De Araujo I.E. Sweet taste signaling functions as a hypothalamic glucose sensor. Front. Integr. Neurosci. 2009, 3:12.
44. Routh V.H. Glucose-sensing neurons: are they physiologically relevant?. Physiol. Behav. 2002, 76:403-413.
45. Rowe I.C., Boden P.R., Ashford M.L. Potassium channel dysfunction in hypothalamic glucose-receptive neurones of obese Zucker rats. J. Physiol. 1996, 497(Pt 2):365-377.
46. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Meth. 2012, 9:671-675.
47. Silver I.A., Erecinska M. Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J. Neurosci. 1994, 14:5068-5076.
48. Silver I.A., Erecinska M. Glucose-induced intracellular ion changes in sugar-sensitive hypothalamic neurons. J. Neurophysiol. 1998, 79:1733-1745.
49. Song Z., Levin B.E., Mcardle J.J., Bakhos N., Routh V.H. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 2001, 50:2673-2681.
50. Thorens B. Sensing of glucose in the brain. Handb. Exp. Pharmacol. 2012, 277-294.
51. Vaandrager A.B., Smolenski A., Tilly B.C., Houtsmuller A.B., Ehlert E.M., Bot A.G., Edixhoven M., Boomaars W.E., Lohmann S.M., De Jonge H.R. Membrane targeting of cGMP-dependent protein kinase is required for cystic fibrosis transmembrane conductance regulator Cl- channel activation. Proc. Natl. Acad. Sci. USA 1998, 95:1466-1471.
52. Wang R., Liu X., Hentges S.T., Dunn-Meynell A.A., Levin B.E., Wang W., Routh V.H. The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 2004, 53:1959-1965.
53. Zhao G.Q., Zhang Y., Hoon M.A., Chandrashekar J., Erlenbach I., Ryba N.J., Zuker C.S. The receptors for mammalian sweet and umami taste. Cell 2003, 115:255-266.