Metabolic regulation of lateral hypothalamic glucose-inhibited orexin neurons may influence midbrain reward neurocircuitry

Molecular and Cellular Neuroscience

Volumn 62, Issue , 2014, Pages 30-41

  Sheng, Zhenyu ^a   Santiago, Ammy M ^a   Thomas, Mark P ^b   Routh, Vanessa H ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NORTHERN COLORADO   (United States)

Author keywords

Dopamine; Electrophysiology; Energy balance; Ghrelin; Leptin; Ventral tegmental area

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; 4 AMINOBUTYRIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUCOSE; GLUTAMIC ACID; LEPTIN; NEUROTENSIN RECEPTOR; OREXIN; CALCIUM CHANNEL; DEOXYGLUCOSE; DOPAMINE; GHRELIN; GREEN FLUORESCENT PROTEIN; LEPTIN RECEPTOR; POTASSIUM CHANNEL; 1-(2-METHYLBENZOXAZOL-6-YL)-3-(1,5)NAPHTHYRIDIN-4-YL UREA; BENZOXAZOLE DERIVATIVE; NEUROPEPTIDE; SIGNAL PEPTIDE; UREA;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ELECTROPHYSIOLOGICAL PROCEDURES; LATERAL HYPOTHALAMUS; MALE; MESENCEPHALON; METABOLIC REGULATION; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REWARD; WHOLE CELL; BRAIN ELECTROPHYSIOLOGY; CELL ACTIVATION; DIET RESTRICTION; GLUCOSE METABOLISM; MEMBRANE POTENTIAL; PROTEIN EXPRESSION; VENTRAL TEGMENTUM; WEIGHT REDUCTION; WHOLE CELL PATCH CLAMP; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BENZOXAZOLES; GLUCOSE; HYPOTHALAMIC AREA, LATERAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MESENCEPHALON; MICE, INBRED C57BL; NEURONS; NEUROPEPTIDES; OREXINS; REWARD; SYNAPTIC TRANSMISSION; UREA; VENTRAL TEGMENTAL AREA;

EID: 84906218386     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2014.08.001     Document Type: Article

References (51)

1. Ahima R.S., Saper C.B., Flier J.S., Elmquist J.K. Leptin regulation of neuroendocrine systems. Front. Neuroendocrinol. 2000, 21:263-307.
2. Antunes V.R., Brailoiu G.C., Kwok E.H., Scruggs P., Dun N.J. Orexins/hypocretins excite rat sympathetic preganglionic neurons in vivo and in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R1801-R1807.
3. Borgland S.L., Taha S.A., Sarti F., Fields H.L., Bonci A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 2006, 49:589-601.
4. Borgland S.L., Chang S.-J., Bowers M.S., Thompson J.L., Vittoz N., Floresco S.B., Chou J., Chen B.T., Bonci A. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J. Neurosci. 2009, 29:11215-11225.
5. Burdakov D., Gerasimenko O., Verkhratsky A. Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J. Neurosci. 2005, 25:2429-2433.
6. + channels mediate inhibition of orexin neurons by glucose. Neuron 2006, 50:711-722.
7. Cai X.J.P.S., Harrold J., Wilson S., Buckingham R.E., Arch J.R., Tadayyon M., Clapham J.C., Wilding J., Williams G. Hypothalamic orexin expression: modulation by blood glucose and feeding. Diabetes 1999, 48:2132-2137.
8. Cason A.M., Smith R.J., Tahsili-Fahadan P., Moorman D.E., Sartor G.C., Aston-Jones G. Role of orexin/hypocretin in reward-seeking and addiction: implications for obesity. Physiol. Behav. 2010, 100:419-428.
9. Cheng S.B., Kuchiiwa S., Gao H.Z., Kuchiiwa T., Nakagawa S. Morphological study of orexin neurons in the hypothalamus of the Long-Evans rat, with special reference to co-expression of orexin and NADPH-diaphorase or nitric oxide synthase activities. Neurosci. Res. 2003, 46:53-62.
10. Chou T.C., Scammell T.E., Gooley J.J., Gaus S.E., Saper C.B., Lu J. Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J. Neurosci. 2003, 23:10691-10702.
11. Cummings D.E., Weigle D.S., Frayo R.S., Breen P.A., Ma M.K., Dellinger E.P., Purnell J.Q. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N. Engl. J. Med. 2002, 346:1623-1630.
12. 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.
13. Diano S., Horvath B., Urbanski H.F., Sotonyi P., Horvath T.L. Fasting activates the nonhuman primate hypocretin (orexin) system and its postsynaptic targets. Endocrinology 2003, 144:3774-3778.
14. Dunn-Meynell A.A., Sanders N.M., Compton D., Becker T.C., Ji Eiki, Zhang B.B., Levin B.E. Relationship among brain and blood glucose levels and spontaneous and glucoprivic feeding. J. Neurosci. 2009, 29:7015-7022.
15. Fields H.L., Hjelmstad G.O., Margolis E.B., Nicola S.M. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu. Rev. Neurosci. 2007, 30:289-316.
16. Fioramonti X., Contie S., Song Z., Routh V.H., Lorsignol A., Penicaud L. Characterization of glucosensing neuron subpopulations in the arcuate nucleus: integration in NPY and POMC networks?. Diabetes 2007, 56:1219-1227.
17. Ford C.P., Mark G.P., Williams J.T. Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J. Neurosci. 2006, 26:2788-2797.
18. Fulton S. Appetite and reward. Front. Neuroendocrinol. 2010, 31:85-103.
19. Gonzalez J.A., Jensen L.T., Fugger L., Burdakov D. Metabolism-independent sugar sensing in central orexin neurons. Diabetes 2008, 57:2569-2576.
20. González J.A., Jensen L.T., Doyle S.E., Miranda-Anaya M., Menaker M., Fugger L., Bayliss D.A., Burdakov D. Deletion of TASK1 and TASK3 channels disrupts intrinsic excitability but does not abolish glucose or pH responses of orexin/hypocretin neurons. Eur. J. Neurosci. 2009, 30:57-64.
21. González J.A., Jensen L.T., Fugger L., Burdakov D. Convergent inputs from electrically and topographically distinct orexin cells to locus coeruleus and ventral tegmental area. Eur. J. Neurosci. 2012, 35:1426-1432.
22. Horvath T.L., Gao X.-B. Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab. 2005, 1:279-286.
23. Horvath T.L., Diano S., van den Pol A.N. Synaptic interaction between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J. Neurosci. 1999, 19:1072-1087.
24. Jiménez A., Caba M., Escobar C. Food-entrained patterns in orexin cells reveal subregion differential activation. Brain Res. 2013, 1513:41-50.
25. Korotkova T.M., Sergeeva O.A., Eriksson K.S., Haas H.L., Brown R.E. Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J. Neurosci. 2003, 23:7-11.
26. Korotkova T.M., Brown R.E., Sergeeva O.A., Ponomarenko A.A., Haas H.L. Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur. J. Neurosci. 2006, 23:2677-2685.
27. Leinninger G.M., Jo Y.-H., Leshan R.L., Louis G.W., Yang H., Barrera J.G., Wilson H., Opland D.M., Faouzi M.A., Gong Y., Jones J.C., Rhodes C.J., Chua S., Diano S., Horvath T.L., Seeley R.J., Becker J.B., Münzberg H., Myers M.G. Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab. 2009, 10:89-98.
28. Leinninger G.M., Opland D.M., Jo Y.-H., Faouzi M., Christensen L., Cappellucci Laura A., Rhodes Christopher J., Gnegy Margaret E., Becker Jill B., Pothos Emmanuel N., Seasholtz Audrey F., Thompson Robert C., Myers Jr Martin G. Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab. 2011, 14:313-323.
29. Levin B.E. Glucose-regulated dopamine release from substantia nigra neurons. Brain Res. 2000, 874:158-164.
30. Li Y., Gao X.B., Sakurai T., van den Pol A.N. Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron-a potential mechanism for orchestrating the hypothalamic arousal system. Neuron 2002, 36(6):1169-1181.
31. Liu Z.-W., Gan G., Suyama S., Gao X.-B. Intracellular energy status regulates activity in hypocretin/orexin neurones: a link between energy and behavioural states. J. Physiol. 2011, 589:4157-4166.
32. López M., Seoane L., del Carmen García M., Lago F., Casanueva F.F., Señarís R., Diéguez C. Leptin regulation of prepro-orexin and orexin receptor mRNA levels in the hypothalamus. Biochem. Biophys. Res. Commun. 2000, 269:41-45.
33. 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 (NPY)-glucose-inhibited (GI) neurons to decreased extracellular glucose. AJP Cell Physiol. 2009, 296:746-756.
34. Nollet M., Gaillard P., Minier F., Tanti A., Belzung C., Leman S. Activation of orexin neurons in dorsomedial/perifornical hypothalamus and antidepressant reversal in a rodent model of depression. Neuropharmacology 2011, 61:336-346.
35. Osterstock G., Escobar P., Mitutsova V., Gouty-Colomer L.A., Fontanaud P., Molino F., Fehrentz J.A., Carmignac D., Martinez J., Guerineau N.C., Robinson I.C., Mollard P., Méry P.F. Ghrelin stimulation of growth hormone-releasing hormone neurons is direct in the arcuate nucleus. PLoS One 2010, 5(2):5. (e9159). 10.1371/journal.pone.0009159.
36. Parsons M.P., Hirasawa M. ATP-sensitive potassium channel-mediated lactate effect on orexin neurons: implications for brain energetics during arousal. J. Neurosci. 2010, 30:8061-8070.
37. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press. 4th ed.
38. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., Kilduff T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 1998, 18:9996-10015.
39. Rosin D.L., Weston M.C., Sevigny C.P., Stornetta R.L., Guyenet P.G. Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J. Comp. Neurol. 2003, 465:593-603.
40. Sakurai T. Roles of orexins in regulation of feeding and wakefulness. NeuroReport 2002, 13:987-995.
41. Sakurai T., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
42. 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.
43. Song Z., Routh V.H. Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 2005, 54:15-22.
44. 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.
45. Spanswick D., Smith M.A., Groppi V.E., Logan S.D., Ashford M.L.J. Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature 1997, 390:521-525.
46. Teske J.A., Levine A.S., Kuskowski M., Levine J.A., Kotz C.M. Elevated hypothalamic orexin signaling, sensitivity to orexin A, and spontaneous physical activity in obesity-resistant rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R889-R899.
47. Tupone D., Madden C.J., Cano G., Morrison S.F. An orexinergic projection from perifornical hypothalamus to raphe pallidus increases rat brown adipose tissue thermogenesis. J. Neurosci. 2011, 31:15944-15955.
48. van den Pol A.N., Gao X.B., Obrietan K., Kilduff T.S., Belousov A.B. Presynaptic and postsynaptic actions and modulation of neuroendocrine neurons by a new hypothalamic peptide, hypocretin/orexin. J. Neurosci. 1998, 18:7962-7971.
49. Vittoz N.M., Schmeichel B., Berridge C.W. Hypocretin/orexin preferentially activates caudomedial ventral tegmental area dopamine neurons. Eur. J. Neurosci. 2008, 28:1629-1640.
50. 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.
51. Yamanaka A., Beuckmann C.T., Willie J.T., Hara J., Tsujino N., Mieda M., Tominaga M., K-i Yagami, Sugiyama F., Goto K., Yanagisawa M., Sakurai T. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 2003, 38:701-713.