Hypothalamic nutrient sensing in the control of energy homeostasis

Behavioural Brain Research

Volumn 209, Issue 1, 2010, Pages 1-12

  Blouet, Clémence ^a   Schwartz, Gary J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Brainstem; Energy balance; Glucose homeostasis; Hypothalamus; Insulin resistance; Lipid metabolism; Nutrient sensing; Obesity

Indexed keywords

GHRELIN; GLUCOSE; INSULIN; LEPTIN; MELANOCORTIN; OREXIN A;

ADIPOSE TISSUE; ANOREXIA; BRAIN FUNCTION; DOPAMINERGIC SYSTEM; ENERGY BALANCE; ENERGY EXPENDITURE; FEEDING BEHAVIOR; FOOD INTAKE; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; HORMONE ACTION; HYPOTHALAMIC NUTRIENT SENSING; HYPOTHALAMUS FUNCTION; HYPOTHALAMUS NUCLEUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; INSULIN RELEASE; METABOLIC DISORDER; METABOLIC REGULATION; NEUROENDOCRINE SYSTEM; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; NUTRIENT AVAILABILITY; NUTRIENT UPTAKE; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE METABOLISM;

ADIPOSE TISSUE; ANIMALS; ENERGY METABOLISM; FEEDING BEHAVIOR; GLUCOSE; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; MODELS, BIOLOGICAL; NERVE NET; NEURAL PATHWAYS; NEURONS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA;

EID: 77249131674     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.12.024     Document Type: Review

References (207)

1. Abbott C.R., Kennedy A.R., Wren A.M., Rossi M., Murphy K.G., Seal L.J., et al. Identification of hypothalamic nuclei involved in the orexigenic effect of melanin-concentrating hormone. Endocrinology 144 (2003) 3943-3949
2. Ainscow E.K., Mirshamsi S., Tang T., Ashford M.L., and Rutter G.A. Dynamic imaging of free cytosolic ATP concentration during fuel sensing by rat hypothalamic neurones: evidence for ATP-independent control of ATP-sensitive K(+) channels. J Physiol 544 (2002) 429-445
3. Aja S., Bi S., Knipp S.B., McFadden J.M., Ronnett G.V., Kuhajda F.P., et al. Intracerebroventricular C75 decreases meal frequency and reduces AgRP gene expression in rats. Am J Physiol Regul Integr Comp Physiol 291 (2006) R148-R154
4. Alquier T., Kawashima J., Tsuji Y., and Kahn B.B. Role of hypothalamic adenosine 5′-monophosphate-activated protein kinase in the impaired counterregulatory response induced by repetitive neuroglucopenia. Endocrinology 148 (2007) 1367-1375
5. Andrews Z.B., Liu Z.W., Walllingford N., Erion D.M., Borok E., Friedman J.M., et al. UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals. Nature 454 (2008) 846-851
6. Ashford M.L., Boden P.R., and Treherne J.M. Glucose-induced excitation of hypothalamic neurones is mediated by ATP-sensitive K+ channels. Pflugers Arch 415 (1990) 479-483
7. Azzara A.V., Sokolnicki J.P., and Schwartz G.J. Central melanocortin receptor agonist reduces spontaneous and scheduled meal size but does not augment duodenal preload-induced feeding inhibition. Physiol Behav 77 (2002) 411-416
8. Bady I., Marty N., Dallaporta M., Emery M., Gyger J., Tarussio D., et al. Evidence from glut2-null mice that glucose is a critical physiological regulator of feeding. Diabetes 55 (2006) 988-995
9. Bagnol D., Lu X.Y., Kaelin C.B., Day H.E., Ollmann M., Gantz I., et al. Anatomy of an endogenous antagonist: relationship between Agouti-related protein and proopiomelanocortin in brain. J Neurosci 19 (1999) RC26
10. Balthasar N., Dalgaard L.T., Lee C.E., Yu J., Funahashi H., Williams T., et al. Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123 (2005) 493-505
11. Benani A., Troy S., Carmona M.C., Fioramonti X., Lorsignol A., Leloup C., et al. Role for mitochondrial reactive oxygen species in brain lipid sensing: redox regulation of food intake. Diabetes 56 (2007) 152-160
12. Benoit S.C., Kemp C.J., Elias C.F., Abplanalp W., Herman J.P., Migrenne S., et al. Palmitic acid mediates hypothalamic insulin resistance by altering PKC-theta subcellular localization in rodents. J Clin Invest 119 (2009) 2577-2589
13. Berthoud H.R. Multiple neural systems controlling food intake and body weight. Neurosci Biobehav Rev 26 (2002) 393-428
14. Berthoud H.R., Patterson L.M., Sutton G.M., Morrison C., and Zheng H. Orexin inputs to caudal raphe neurons involved in thermal, cardiovascular, and gastrointestinal regulation. Histochem Cell Biol 123 (2005) 147-156
15. Berthoud H.R., Sutton G.M., Townsend R.L., Patterson L.M., and Zheng H. Brainstem mechanisms integrating gut-derived satiety signals and descending forebrain information in the control of meal size. Physiol Behav 89 (2006) 517-524
16. Biggers D.W., Myers S.R., Neal D., Stinson R., Cooper N.B., Jaspan J.B., et al. Role of brain in counterregulation of insulin-induced hypoglycemia in dogs. Diabetes 38 (1989) 7-16
17. Bingham N.C., Anderson K.K., Reuter A.L., Stallings N.R., and Parker K.L. Selective loss of leptin receptors in the ventromedial hypothalamic nucleus results in increased adiposity and a metabolic syndrome. Endocrinology 149 (2008) 2138-2148
18. Blevins J.E., Eakin T.J., Murphy J.A., Schwartz M.W., and Baskin D.G. Oxytocin innervation of caudal brainstem nuclei activated by cholecystokinin. Brain Res 993 (2003) 30-41
19. Blevins J.E., Schwartz M.W., and Baskin D.G. Evidence that paraventricular nucleus oxytocin neurons link hypothalamic leptin action to caudal brain stem nuclei controlling meal size. Am J Physiol Regul Integr Comp Physiol 287 (2004) R87-R96
20. Blouet C., Jo Y.H., Li X., and Schwartz G.J. Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus-brainstem circuit. J Neurosci 29 (2009) 8302-8311
21. Blouet C., Ono H., and Schwartz G.J. Mediobasal hypothalamic p70 S6 kinase 1 modulates the control of energy homeostasis. Cell Metab 8 (2008) 459-467
22. Borg W.P., Sherwin R.S., During M.J., Borg M.A., and Shulman G.I. Local ventromedial hypothalamus glucopenia triggers counterregulatory hormone release. Diabetes 44 (1995) 180-184
23. Brito M.N., Brito N.A., Baro D.J., Song C.K., and Bartness T.J. Differential activation of the sympathetic innervation of adipose tissues by melanocortin receptor stimulation. Endocrinology 148 (2007) 5339-5347
24. Brito N.A., Brito M.N., and Bartness T.J. Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am J Physiol Regul Integr Comp Physiol 294 (2008) R1445-R1452
25. Broberger C., De Lecea L., Sutcliffe J.G., and Hokfelt T. Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402 (1998) 460-474
26. Buettner C., Muse E.D., Cheng A., Chen L., Scherer T., Pocai A., et al. Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat Med 14 (2008) 667-675
27. Buettner C., Pocai A., Muse E.D., Etgen A.M., Myers Jr. M.G., and Rossetti L. Critical role of STAT3 in leptin's metabolic actions. Cell Metab 4 (2006) 49-60
28. Burdakov D., Luckman S.M., and Verkhratsky A. Glucose-sensing neurons of the hypothalamus. Philos Trans R Soc Lond B Biol Sci 360 (2005) 2227-2235
29. Cailotto C., van Heijningen C., van der Vliet J., van der Plasse G., Habold C., Kalsbeek A., et al. Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology 149 (2008) 1914-1925
30. Campfield L.A., Brandon P., and Smith F.J. On-line continuous measurement of blood glucose and meal pattern in free-feeding rats: the role of glucose in meal initiation. Brain Res Bull 14 (1985) 605-616
31. Cannon B., and Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 84 (2004) 277-359
32. Canteras N.S., Simerly R.B., and Swanson L.W. Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 348 (1994) 41-79
33. Cha S.H., Wolfgang M., Tokutake Y., Chohnan S., and Lane M.D. Differential effects of central fructose and glucose on hypothalamic malonyl-CoA and food intake. Proc Natl Acad Sci USA 105 (2008) 16871-16875
34. Chen A.S., Marsh D.J., Trumbauer M.E., Frazier E.G., Guan X.M., Yu H., et al. Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat Genet 26 (2000) 97-102
35. Chen A.S., Metzger J.M., Trumbauer M.E., Guan X.M., Yu H., Frazier E.G., et al. Role of the melanocortin-4 receptor in metabolic rate and food intake in mice. Transgenic Res 9 (2000) 145-154
36. Claret M., Smith M.A., Batterham R.L., Selman C., Choudhury A.I., Fryer L.G., et al. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J Clin Invest 117 (2007) 2325-2336
37. Clegg D.J., Wortman M.D., Benoit S.C., McOsker C.C., and Seeley R.J. Comparison of central and peripheral administration of C75 on food intake, body weight, and conditioned taste aversion. Diabetes 51 (2002) 3196-3201
38. Clement L., Cruciani-Guglielmacci C., Magnan C., Vincent M., Douared L., Orosco M., et al. Intracerebroventricular infusion of a triglyceride emulsion leads to both altered insulin secretion and hepatic glucose production in rats. Pflugers Arch 445 (2002) 375-380
39. Collin M., Backberg M., Ovesjo M.L., Fisone G., Edwards R.H., Fujiyama F., et al. Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight. Eur J Neurosci 18 (2003) 1265-1278
40. Colombani A.L., Carneiro L., Benani A., Galinier A., Jaillard T., Duparc T., et al. Enhanced hypothalamic glucose sensing in obesity: alteration of redox signalling. Diabetes 58 (2009) 2189-2197
41. Cone R.D. Anatomy and regulation of the central melanocortin system. Nat Neurosci 8 (2005) 571-578
42. Cota D., Proulx K., Smith K.A., Kozma S.C., Thomas G., Woods S.C., et al. Hypothalamic mTOR signalling regulates food intake. Science 312 (2006) 927-930
43. Cotero V.E., and Routh V.H. Insulin blunts the response of glucose-excited neurons in the ventrolateral-ventromedial hypothalamic nucleus to decreased glucose. Am J Physiol Endocrinol Metab 296 (2009) E1101-E1109
44. Cowley M.A., Pronchuk N., Fan W., Dinulescu D.M., Colmers W.F., and Cone R.D. Integration of NPY, AGRP, and melanocortin signals in the hypothalamic paraventricular nucleus: evidence of a cellular basis for the adipostat. Neuron 24 (1999) 155-163
45. Cruciani-Guglielmacci C., Hervalet A., Douared L., Sanders N.M., Levin B.E., Ktorza A., et al. Beta oxidation in the brain is required for the effects of non-esterified fatty acids on glucose-induced insulin secretion in rats. Diabetologia 47 (2004) 2032-2038
46. Daniels D., Patten C.S., Roth J.D., Yee D.K., and Fluharty S.J. Melanocortin receptor signalling through mitogen-activated protein kinase in vitro and in rat hypothalamus. Brain Res 986 (2003) 1-11
47. Dey D., Basu D., Roy S.S., Bandyopadhyay A., and Bhattacharya S. Involvement of novel PKC isoforms in FFA induced defects in insulin signalling. Mol Cell Endocrinol 246 (2006) 60-64
48. Dunn-Meynell A.A., Govek E., and Levin B.E. Intracarotid glucose selectively increases Fos-like immunoreactivity in paraventricular, ventromedial and dorsomedial nuclei neurons. Brain Res 748 (1997) 100-106
49. Dunn-Meynell A.A., Routh V.H., Kang L., Gaspers L., and Levin B.E. Glucokinase is the likely mediator of glucosensing in both glucose-excited and glucose-inhibited central neurons. Diabetes 51 (2002) 2056-2065
50. Dunn-Meynell A.A., Sanders N.M., Compton D., Becker T.C., Eiki J., Zhang B.B., et al. Relationship among brain and blood glucose levels and spontaneous and glucoprivic feeding. J Neurosci 29 (2009) 7015-7022
51. Elmquist J.K., Coppari R., Balthasar N., Ichinose M., and Lowell B.B. Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J Comp Neurol 493 (2005) 63-71
52. Erickson J.C., Clegg K.E., and Palmiter R.D. Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381 (1996) 415-421
53. Escartin C., Pierre K., Colin A., Brouillet E., Delzescaux T., Guillermier M., et al. Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J Neurosci 27 (2007) 7094-7104
54. Evans M.L., McCrimmon R.J., Flanagan D.E., Keshavarz T., Fan X., McNay E.C., et al. Hypothalamic ATP-sensitive K+ channels play a key role in sensing hypoglycemia and triggering counterregulatory epinephrine and glucagon responses. Diabetes 53 (2004) 2542-2551
55. Fan W., Morrison S.F., Cao W.H., and Yu P. Thermogenesis activated by central melanocortin signalling is dependent on neurons in the rostral raphe pallidus (rRPa) area. Brain Res 1179 (2007) 61-69
56. Fioramonti X., Contie S., Song Z., Routh V.H., Lorsignol A., and Penicaud L. Characterization of glucosensing neuron subpopulations in the arcuate nucleus: integration in neuropeptide Y and pro-opio melanocortin networks?. Diabetes 56 (2007) 1219-1227
57. Fioramonti X., Lorsignol A., Taupignon A., and Penicaud L. A new ATP-sensitive K+ channel-independent mechanism is involved in glucose-excited neurons of mouse arcuate nucleus. Diabetes 53 (2004) 2767-2775
58. Foster M.T., Song C.K., and Bartness T.J. Hypothalamic paraventricular nucleus lesion involvement in the sympathetic control of lipid mobilization. SO-Obesity (2009) [Epub ahead of print]
59. Frizzell R.T., Jones E.M., Davis S.N., Biggers D.W., Myers S.R., Connolly C.C., et al. Counterregulation during hypoglycemia is directed by widespread brain regions. Diabetes 42 (1993) 1253-1261
60. Fu L.Y., Acuna-Goycolea C., and van den Pol A.N. Neuropeptide Y inhibits hypocretin/orexin neurons by multiple presynaptic and postsynaptic mechanisms: tonic depression of the hypothalamic arousal system. J Neurosci 24 (2004) 8741-8751
61. Fu L.Y., and van den Pol A.N. Agouti-related peptide and MC3/4 receptor agonists both inhibit excitatory hypothalamic ventromedial nucleus neurons. J Neurosci 28 (2008) 5433-5449
62. Gao S., and Lane M.D. Effect of the anorectic fatty acid synthase inhibitor C75 on neuronal activity in the hypothalamus and brainstem. Proc Natl Acad Sci USA 100 (2003) 5628-5633
63. Georgescu D., Sears R.M., Hommel J.D., Barrot M., Bolanos C.A., Marsh D.J., et al. The hypothalamic neuropeptide melanin-concentrating hormone acts in the nucleus accumbens to modulate feeding behavior and forced-swim performance. J Neurosci 25 (2005) 2933-2940
64. German J., Kim F., Schwartz G.J., Havel P.J., Rhodes C.J., Schwartz M.W., et al. Hypothalamic leptin signalling regulates hepatic insulin sensitivity via a neurocircuit involving the vagus nerve. Endocrinology 150 (2009) 4502-4511
65. Glick M., Segal-Lieberman G., Cohen R., and Kronfeld-Schor N. Chronic MCH infusion causes a decrease in energy expenditure and body temperature, and an increase in serum IGF-1 levels in mice. Endocrine (2009) [Epub ahead of print]
66. Gonzalez J.A., Jensen L.T., Fugger L., and Burdakov D. Metabolism-independent sugar sensing in central orexin neurons. Diabetes 57 (2008) 2569-2576
67. Grill H.J., Ginsberg A.B., Seeley R.J., and Kaplan J.M. Brainstem application of melanocortin receptor ligands produces long-lasting effects on feeding and body weight. J Neurosci 18 (1998) 10128-10135
68. Gropp E., Shanabrough M., Borok E., Xu A.W., Janoschek R., Buch T., et al. Agouti-related peptide-expressing neurons are mandatory for feeding. Nat Neurosci 8 (2005) 1289-1291
69. Guesdon B., Paradis E., Samson P., and Richard D. Effects of intracerebroventricular and intra-accumbens melanin-concentrating hormone agonism on food intake and energy expenditure. Am J Physiol Regul Integr Comp Physiol 296 (2009) R469-R475
70. Han S.M., Namkoong C., Jang P.G., Park I.S., Hong S.W., Katakami H., et al. Hypothalamic AMP-activated protein kinase mediates counter-regulatory responses to hypoglycaemia in rats. Diabetologia 48 (2005) 2170-2178
71. Hayes M.R., Skibicka K.P., Bence K.K., and Grill H.J. Dorsal hindbrain 5′-adenosine monophosphate-activated protein kinase as an intracellular mediator of energy balance. Endocrinology 150 (2009) 2175-2182
72. Haynes W.G., Morgan D.A., Walsh S.A., Mark A.L., and Sivitz W.I. Receptor-mediated regional sympathetic nerve activation by leptin. J Clin Invest 100 (1997) 270-278
73. He B., White B.D., Edwards G.L., and Martin R.J. Neuropeptide Y antibody attenuates 2-deoxy-d-glucose induced feeding in rats. Brain Res 781 (1998) 348-350
74. He W., Lam T.K., Obici S., and Rossetti L. Molecular disruption of hypothalamic nutrient sensing induces obesity. Nat Neurosci 9 (2006) 227-233
75. Hentges S.T., Nishiyama M., Overstreet L.S., Stenzel-Poore M., Williams J.T., and Low M.J. GABA release from proopiomelanocortin neurons. J Neurosci 24 (2004) 1578-1583
76. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 444 (2006) 860-867
77. Hu Z., Cha S.H., van Haasteren G., Wang J., and Lane M.D. Effect of centrally administered C75, a fatty acid synthase inhibitor, on ghrelin secretion and its downstream effects. Proc Natl Acad Sci USA 102 (2005) 3972-3977
78. Huszar D., Lynch C.A., Fairchild-Huntress V., Dunmore J.H., Fang Q., Berkemeier L.R., et al. Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88 (1997) 131-141
79. Hutson S.M., Berkich D., Drown P., Xu B., Aschner M., and LaNoue K.F. Role of branched-chain aminotransferase isoenzymes and gabapentin in neurotransmitter metabolism. J Neurochem 71 (1998) 863-874
80. Ibrahim N., Bosch M.A., Smart J.L., Qiu J., Rubinstein M., Ronnekleiv O.K., et al. Hypothalamic proopiomelanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology 144 (2003) 1331-1340
81. Jo Y.H., Su Y., Gutierrez-Juarez R., and Chua Jr. S. Oleic acid directly regulates POMC neuron excitability in the hypothalamus. J Neurophysiol 101 (2009) 2305-2316
82. Johnstone L.E., Fong T.M., and Leng G. Neuronal activation in the hypothalamus and brainstem during feeding in rats. Cell Metab 4 (2006) 313-321
83. Kalsbeek A., La Fleur S., Van Heijningen C., and Buijs R.M. Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 24 (2004) 7604-7613
84. Kang L., Dunn-Meynell A.A., Routh V.H., Gaspers L.D., Nagata Y., Nishimura T., et al. Glucokinase is a critical regulator of ventromedial hypothalamic neuronal glucosensing. Diabetes 55 (2006) 412-420
85. Kang L., Routh V.H., Kuzhikandathil E.V., Gaspers L.D., and Levin B.E. Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 53 (2004) 549-559
86. Kang L., Sanders N.M., Dunn-Meynell A.A., Gaspers L.D., Routh V.H., Thomas A.P., et al. Prior hypoglycemia enhances glucose responsiveness in some ventromedial hypothalamic glucosensing neurons. Am J Physiol Regul Integr Comp Physiol 294 (2008) R784-R792
87. Kawano H., and Masuko S. Beta-endorphin-, adrenocorticotrophic hormone- and neuropeptide y-containing projection fibers from the arcuate hypothalamic nucleus make synaptic contacts on to nucleus preopticus medianus neurons projecting to the paraventricular hypothalamic nucleus in the rat. Neuroscience 98 (2000) 555-565
88. Kim K.W., Zhao L., and Parker K.L. Central nervous system-specific knockout of steroidogenic factor 1. Mol Cell Endocrinol 300 (2009) 132-136
89. Kohno D., Sone H., Minokoshi Y., and Yada T. Ghrelin raises [Ca2+]i via AMPK in hypothalamic arcuate nucleus NPY neurons. Biochem Biophys Res Commun 366 (2008) 388-392
90. Kokoeva M.V., Yin H., and Flier J.S. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310 (2005) 679-683
91. Kokoeva M.V., Yin H., and Flier J.S. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505 (2007) 209-220
92. Kokorovic A., Cheung G.W., Rossetti L., and Lam T.K. Hypothalamic sensing of circulating lactate regulates glucose production. J Cell Mol Med 255 (2008) 28-36
93. Konner A.C., Janoschek R., Plum L., Jordan S.D., Rother E., Ma X., et al. Insulin action in AgRP-expressing neurons is required for suppression of hepatic glucose production. Cell Metab 5 (2007) 438-449
94. Kublaoui B.M., Gemelli T., Tolson K.P., Wang Y., and Zinn A.R. Oxytocin deficiency mediates hyperphagic obesity of Sim1 haploinsufficient mice. Mol Endocrinol 22 (2008) 1723-1734
95. Kumar M.V., Shimokawa T., Nagy T.R., and Lane M.D. Differential effects of a centrally acting fatty acid synthase inhibitor in lean and obese mice. Proc Natl Acad Sci USA 99 (2002) 1921-1925
96. Kurata K., Fujimoto K., Sakata T., Etou H., and Fukagawa K. d-Glucose suppression of eating after intra-third ventricle infusion in rat. Physiol Behav 37 (1986) 615-620
97. Lam C.K., Chari M., Wang P.Y., and Lam T.K. Central lactate metabolism regulates food intake. Am J Physiol Endocrinol Metab 295 (2008) E491-E496
98. Lam T.K., Gutierrez-Juarez R., Pocai A., Bhanot S., Tso P., Schwartz G.J., et al. Brain glucose metabolism controls the hepatic secretion of triglyceride-rich lipoproteins. Nat Med 13 (2007) 171-180
99. Lam T.K., Gutierrez-Juarez R., Pocai A., and Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science 309 (2005) 943-947
100. Lam T.K., Pocai A., Gutierrez-Juarez R., Obici S., Bryan J., Aguilar-Bryan L., et al. Hypothalamic sensing of circulating fatty acids is required for glucose homeostasis. Nat Med 11 (2005) 320-327
101. Landgraf R., Malkinson T., Horn T., Veale W.L., Lederis K., and Pittman Q.J. Release of vasopressin and oxytocin by paraventricular stimulation in rats. Am J Physiol 258 (1990) R155-R159
102. Lane M.D., Wolfgang M., Cha S.H., and Dai Y. Regulation of food intake and energy expenditure by hypothalamic malonyl-CoA. Int J Obes (Lond) 32 (2008) S49-S54
103. Le Foll C., Irani B.G., Magnan C., Dunn-Meynell A.A., and Levin B.E. Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. Am J Physiol Regul Integr Comp Physiol 297 (2009) R655-R664
104. Le Foll C., Irani B.G., Magnan C., Dunn-Meynell A.A., and Levin B.E. Effects of maternal genotype and diet on offspring glucose and fatty acid sensing ventromedial hypothalamic nucleus neurons. Am J Physiol Regul Integr Comp Physiol 297 5 (2009) R1351-R1357
105. 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 55 (2006)
106. Levin B.E. Metabolic sensing neurons and the control of energy homeostasis. Physiol Behav 89 (2006) 486-489
107. Li L.F., Lu Y.Y., Xiong W., Liu J.Y., and Chen Q. Effect of centrally administered C75, a fatty acid synthase inhibitor, on gastric emptying and gastrointestinal transit in mice. Eur J Pharmacol 595 (2008) 90-94
108. Li Y., Soos T.J., Li X., Wu J., Degennaro M., Sun X., et al. Protein kinase C Theta inhibits insulin signalling by phosphorylating IRS1 at Ser(1101). J Biol Chem 279 (2004) 45304-45307
109. Lin J., Choi Y.H., Hartzell D.L., Li C., Della-Fera M.A., and Baile C.A. CNS melanocortin and leptin effects on stearoyl-CoA desaturase-1 and resistin expression. Biochem Biophys Res Commun 311 (2003) 324-328
110. Loftus T.M., Jaworsky D.E., Frehywot G.L., Townsend C.A., Ronnett G.V., Lane M.D., et al. Reduced food intake and body weight in mice treated with fatty acid synthase inhibitors. Science 288 (2000) 2379-2381
111. Lokrantz C.M., Uvnas-Moberg K., and Kaplan J.M. Effects of central oxytocin administration on intraoral intake of glucose in deprived and nondeprived rats. Physiol Behav 62 (1997) 347-352
112. Ludwig D.S., Tritos N.A., Mastaitis J.W., Kulkarni R., Kokkotou E., Elmquist J., et al. Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107 (2001) 379-386
113. Luquet S., Perez F.A., Hnasko T.S., and Palmiter R.D. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310 (2005) 683-685
114. Lyons W.E., Mamounas L.A., Ricaurte G.A., Coppola V., Reid S.W., Bora S.H., et al. Brain-derived neurotrophic factor-deficient mice develop aggressiveness and hyperphagia in conjunction with brain serotonergic abnormalities. Proc Natl Acad Sci USA 96 (1999) 15239-15244
115. Ma X., Zubcevic L., Bruning J.C., Ashcroft F.M., and Burdakov D. Electrical inhibition of identified anorexigenic POMC neurons by orexin/hypocretin. J Neurosci 27 (2007) 1529-1533
116. MacDonald P.E., Joseph J.W., and Rorsman P. Glucose-sensing mechanisms in pancreatic beta-cells. Philos Trans R Soc Lond B Biol Sci 360 (2005) 2211-2225
117. Maejima Y., Sedbazar U., Suyama S., Kohno D., Onaka T., Takano E., et al. Nesfatin-1-regulated oxytocinergic signalling in the paraventricular nucleus causes anorexia through a leptin-independent melanocortin pathway. Cell Metab 10 (2009) 355-365
118. Magnan C., Collins S., Berthault M.F., Kassis N., Vincent M., Gilbert M., et al. Lipid infusion lowers sympathetic nervous activity and leads to increased beta-cell responsiveness to glucose. J Clin Invest 103 (1999) 413-419
119. Majdic G., Young M., Gomez-Sanchez E., Anderson P., Szczepaniak L.S., Dobbins R.L., et al. Knockout mice lacking steroidogenic factor 1 are a novel genetic model of hypothalamic obesity. Endocrinology 143 (2002) 607-614
120. Marsollier N., Kassis N., Mezghenna K., Soty M., Fioramonti X., Lacombe A., et al. Deregulation of hepatic insulin sensitivity induced by central lipid infusion in rats is mediated by nitric oxide. PLoS One 4 (2009) e6649
121. McClellan K.M., Parker K.L., and Tobet S. Development of the ventromedial nucleus of the hypothalamus. Front Neuroendocrinol 27 (2006) 193-209
122. McCrimmon R.J., Evans M.L., Fan X., McNay E.C., Chan O., Ding Y., et al. Activation of ATP-sensitive K+ channels in the ventromedial hypothalamus amplifies counterregulatory hormone responses to hypoglycemia in normal and recurrently hypoglycemic rats. Diabetes 54 (2005) 3169-3174
123. Melanson K.J., Westerterp-Plantenga M.S., Saris W.H., Smith F.J., and Campfield L.A. Blood glucose patterns and appetite in time-blinded humans: carbohydrate versus fat. Am J Physiol 277 (1999) R337-345
124. Miki T., Liss B., Minami K., Shiuchi T., Saraya A., Kashima Y., et al. ATP-sensitive K+ channels in the hypothalamus are essential for the maintenance of glucose homeostasis. Nat Neurosci 4 (2001) 507-512
125. Miller I., Ronnett G.V., Moran T.H., and Aja S. Anorexigenic C75 alters c-Fos in mouse hypothalamic and hindbrain subnuclei. Neuroreport 15 (2004) 925-929
126. Minokoshi Y., Alquier T., Furukawa N., Kim Y.B., Lee A., Xue B., et al. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428 (2004) 569-574
127. Miselis R.R., and Epstein A.N. Feeding induced by intracerebroventricular 2-deoxy-d-glucose in the rat. Am J Physiol 229 (1975) 1438-1447
128. Moran T.H., Ladenheim E.E., and Schwartz G.J. Within-meal gut feedback signalling. Int J Obes Relat Metab Disord 25 Suppl. 5 (2001) S39-S41
129. Morrison C.D., Xi X., White C.L., Ye J., and Martin R.J. Amino acids inhibit Agrp gene expression via an mTOR-dependent mechanism. Am J Physiol Endocrinol Metab 293 (2007) E165-E171
130. Morton G.J., Cummings D.E., Baskin D.G., Barsh G.S., and Schwartz M.W. Central nervous system control of food intake and body weight. Nature 443 (2006) 289-295
131. Mounien L., Bizet P., Boutelet I., Vaudry H., and Jegou S. Expression of melanocortin MC3 and MC4 receptor mRNAs by neuropeptide Y neurons in the rat arcuate nucleus. Neuroendocrinology 82 (2005) 164-170
132. Mountjoy K.G., Mortrud M.T., Low M.J., Simerly R.B., and Cone R.D. Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol 8 (1994) 1298-1308
133. Mountjoy P.D., Bailey S.J., and Rutter G.A. Inhibition by glucose or leptin of hypothalamic neurons expressing neuropeptide Y requires changes in AMP-activated protein kinase activity. Diabetologia 50 (2007) 168-177
134. Muroya S., Funahashi H., Yamanaka A., Kohno D., Uramura K., Nambu T., et al. Orexins (hypocretins) directly interact with neuropeptide Y, POMC and glucose-responsive neurons to regulate Ca 2+ signalling in a reciprocal manner to leptin: orexigenic neuronal pathways in the mediobasal hypothalamus. Eur J Neurosci 19 (2004) 1524-1534
135. Muroya S., Yada T., Shioda S., and Takigawa M. Glucose-sensitive neurons in the rat arcuate nucleus contain neuropeptide Y. Neurosci Lett 264 (1999) 113-116
136. Murphy B.A., Fioramonti X., Jochnowitz N., Fakira K., Gagen K., Contie S., et al. Fasting enhances the response of arcuate neuropeptide Y-glucose-inhibited neurons to decreased extracellular glucose. Am J Physiol Cell Physiol 296 (2009) C746-C756
137. Nogueiras R., Wiedmer P., Perez-Tilve D., Veyrat-Durebex C., Keogh J.M., Sutton G.M., et al. The central melanocortin system directly controls peripheral lipid metabolism. J Clin Invest 117 (2007) 3475-3488
138. O'Malley D., Reimann F., Simpson A.K., and Gribble F.M. Sodium-coupled glucose cotransporters contribute to hypothalamic glucose sensing. Diabetes 55 (2006) 3381-3386
139. Obici S., Feng Z., Arduini A., Conti R., and Rossetti L. Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat Med 9 (2003) 756-761
140. Obici S., Feng Z., Morgan K., Stein D., Karkanias G., and Rossetti L. Central administration of oleic acid inhibits glucose production and food intake. Diabetes 51 (2002) 271-275
141. Obici S., Zhang B.B., Karkanias G., and Rossetti L. Hypothalamic insulin signalling is required for inhibition of glucose production. Nat Med 8 (2002) 1376-1382
142. Ono H., Pocai A., Wang Y., Sakoda H., Asano T., Backer J.M., et al. Activation of hypothalamic S6 kinase mediates diet-induced hepatic insulin resistance in rats. J Clin Invest 118 (2008) 2959-2968
143. Oomura Y., Ono T., Ooyama H., and Wayner M.J. Glucose and osmosensitive neurones of the rat hypothalamus. Nature 222 (1969) 282-284
144. Palkovits M. Interconnections between the neuroendocrine hypothalamus and the central autonomic system. Geoffrey Harris Memorial Lecture, Kitakyushu, Japan, October 1998. Front Neuroendocrinol 20 (1999) 270-295
145. Parker R.M., and Herzog H. Regional distribution of Y-receptor subtype mRNAs in rat brain. Eur J Neurosci 11 (1999) 1431-1448
146. Parton L.E., Ye C.P., Coppari R., Enriori P.J., Choi B., Zhang C.Y., et al. Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity. Nature 449 (2007) 228-232
147. Pellerin L. Lactate as a pivotal element in neuron-glia metabolic cooperation. Neurochem Int 43 (2003) 331-338
148. Penicaud L., Leloup C., Fioramonti X., Lorsignol A., and Benani A. Brain glucose sensing: a subtle mechanism. Curr Opin Clin Nutr Metab Care 9 (2006) 458-462
149. Plum L., Ma X., Hampel B., Balthasar N., Coppari R., Munzberg H., et al. Enhanced PIP3 signalling in POMC neurons causes KATP channel activation and leads to diet-sensitive obesity. J Clin Invest 116 (2006) 1886-1901
150. Pocai A., Lam T.K., Gutierrez-Juarez R., Obici S., Schwartz G.J., Bryan J., et al. Hypothalamic K(ATP) channels control hepatic glucose production. Nature 434 (2005) 1026-1031
151. Pocai A., Lam T.K., Obici S., Gutierrez-Juarez R., Muse E.D., Arduini A., et al. Restoration of hypothalamic lipid sensing normalizes energy and glucose homeostasis in overfed rats. J Clin Invest 116 (2006) 1081-1091
152. Pocai A., Obici S., Schwartz G.J., and Rossetti L. A brain-liver circuit regulates glucose homeostasis. Cell Metab 1 (2005) 53-61
153. Qian S., Chen H., Weingarth D., Trumbauer M.E., Novi D.E., Guan X., et al. Neither agouti-related protein nor neuropeptide Y is critically required for the regulation of energy homeostasis in mice. Mol Cell Biol 22 (2002) 5027-5035
154. Rahmouni K., Haynes W.G., Morgan D.A., and Mark A.L. Role of melanocortin-4 receptors in mediating renal sympathoactivation to leptin and insulin. J Neurosci 23 (2003) 5998-6004
155. Raposinho P.D., Pierroz D.D., Broqua P., White R.B., Pedrazzini T., and Aubert M.L. Chronic administration of neuropeptide Y into the lateral ventricle of C57BL/6J male mice produces an obesity syndrome including hyperphagia, hyperleptinemia, insulin resistance, and hypogonadism. Mol Cell Endocrinol 185 (2001) 195-204
156. Ren X., Zhou L., Terwilliger R., Newton S.S., and de Araujo I.E. Sweet taste signalling functions as a hypothalamic glucose sensor. Front Integr Neurosci 3 (2009) 12
157. Ross R., Wang P.Y., Chari M., Lam C.K., Caspi L., Ono H., et al. Hypothalamic protein kinase C regulates glucose production. Diabetes 57 (2008) 2061-2065
158. Ryu K.Y., Garza J.C., Lu X.Y., Barsh G.S., and Kopito R.R. Hypothalamic neurodegeneration and adult-onset obesity in mice lacking the Ubb polyubiquitin gene. Proc Natl Acad Sci USA 105 (2008) 4016-4021
159. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8 (2007) 171-181
160. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (1998) 573-585
161. Sanders N.M., Dunn-Meynell A.A., and Levin B.E. Third ventricular alloxan reversibly impairs glucose counterregulatory responses. Diabetes 53 (2004) 1230-1236
162. Satoh N., Ogawa Y., Katsuura G., Numata Y., Tsuji T., Hayase M., et al. Sympathetic activation of leptin via the ventromedial hypothalamus: leptin-induced increase in catecholamine secretion. Diabetes 48 (1999) 1787-1793
163. Sawchenko P.E. Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res 437 (1987) 253-263
164. Sclafani A., Berner C.N., and Maul G. Multiple knife cuts between the medial and lateral hypothalamus in the rat: a reevaluation of hypothalamic feeding circuitry. J Comp Physiol Psychol 88 (1975) 201-207
165. Segal-Lieberman G., Bradley R.L., Kokkotou E., Carlson M., Trombly D.J., Wang X., et al. Melanin-concentrating hormone is a critical mediator of the leptin-deficient phenotype. Proc Natl Acad Sci USA 100 (2003) 10085-10090
166. Sindelar D.K., Ste Marie L., Miura G.I., Palmiter R.D., McMinn J.E., Morton G.J., et al. Neuropeptide Y is required for hyperphagic feeding in response to neuroglucopenia. Endocrinology 145 (2004) 3363-3368
167. Skibicka K.P., and Grill H.J. Energetic responses are triggered by caudal brainstem melanocortin receptor stimulation and mediated by local sympathetic effector circuits. Endocrinology 149 (2008) 3605-3616
168. Skibicka K.P., and Grill H.J. Hypothalamic and hindbrain melanocortin receptors contribute to the feeding, thermogenic and cardiovascular action of melanocortins. Endocrinology 150 12 (2009) 5351-5361
169. Smith M.A., Hisadome K., Al-Qassab H., Heffron H., Withers D.J., and Ashford M.L. Melanocortins and agouti-related protein modulate the excitability of two arcuate nucleus neuron populations by alteration of resting potassium conductances. J Physiol 578 (2007) 425-438
170. Song C.K., Vaughan C.H., Keen-Rhinehart E., Harris R.B., Richard D., and Bartness T.J. Melanocortin-4 receptor mRNA expressed in sympathetic outflow neurons to brown adipose tissue: neuroanatomical and functional evidence. Am J Physiol Regul Integr Comp Physiol 295 (2008) R417-R428
171. Song Z., Levin B.E., McArdle J.J., Bakhos N., and Routh V.H. Convergence of pre- and postsynaptic influences on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 50 (2001) 2673-2681
172. Song Z., and Routh V.H. Differential effects of glucose and lactate on glucosensing neurons in the ventromedial hypothalamic nucleus. Diabetes 54 (2005) 15-22
173. Spanswick D., Smith M.A., Groppi V.E., Logan S.D., and Ashford M.L. Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature 390 (1997) 521-525
174. Spanswick D., Smith M.A., Mirshamsi S., Routh V.H., and Ashford M.L. Insulin activates ATP-sensitive K+ channels in hypothalamic neurons of lean, but not obese rats. Nat Neurosci 3 (2000) 757-758
175. Ste Marie L., Luquet S., Cole T.B., and Palmiter R.D. Modulation of neuropeptide Y expression in adult mice does not affect feeding. Proc Natl Acad Sci USA 102 (2005) 18632-18637
176. Ste Marie L., Miura G.I., Marsh D.J., Yagaloff K., and Palmiter R.D. A metabolic defect promotes obesity in mice lacking melanocortin-4 receptors. Proc Natl Acad Sci USA 97 (2000) 12339-12344
177. Sternson S.M., Shepherd G.M., and Friedman J.M. Topographic mapping of VMH → arcuate nucleus microcircuits and their reorganization by fasting. Nat Neurosci 8 (2005) 1356-1363
178. Sutton G.M., Duos B., Patterson L.M., and Berthoud H.R. Melanocortinergic modulation of cholecystokinin-induced suppression of feeding through extracellular signal-regulated kinase signalling in rat solitary nucleus. Endocrinology 146 (2005) 3739-3747
179. Sutton G.M., Patterson L.M., and Berthoud H.R. Extracellular signal-regulated kinase 1/2 signalling pathway in solitary nucleus mediates cholecystokinin-induced suppression of food intake in rats. J Neurosci 24 (2004) 10240-10247
180. Sutton G.M., Perez-Tilve D., Nogueiras R., Fang J., Kim J.K., Cone R.D., et al. The melanocortin-3 receptor is required for entrainment to meal intake. J Neurosci 28 (2008) 12946-12955
181. Tajima D., Masaki T., Hidaka S., Kakuma T., Sakata T., and Yoshimatsu H. Acute central infusion of leptin modulates fatty acid mobilization by affecting lipolysis and mRNA expression for uncoupling proteins. Exp Biol Med (Maywood) 230 (2005) 200-206
182. Tong Q., Ye C., McCrimmon R.J., Dhillon H., Choi B., Kramer M.D., et al. Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglycemia. Cell Metab 5 (2007) 383-393
183. Tong Q., Ye C.P., Jones J.E., Elmquist J.K., and Lowell B.B. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nat Neurosci 11 (2008) 998-1000
184. Unger T.J., Calderon G.A., Bradley L.C., Sena-Esteves M., and Rios M. Selective deletion of Bdnf in the ventromedial and dorsomedial hypothalamus of adult mice results in hyperphagic behavior and obesity. J Neurosci 27 (2007) 14265-14274
185. van den Top M., Lee K., Whyment A.D., Blanks A.M., and Spanswick D. Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7 (2004) 493-494
186. Wan S., Browning K.N., Coleman F.H., Sutton G., Zheng H., Butler A., et al. Presynaptic melanocortin-4 receptors on vagal afferent fibers modulate the excitability of rat nucleus tractus solitarius neurons. J Neurosci 28 (2008) 4957-4966
187. Wang C., Bomberg E., Levine A., Billington C., and Kotz C.M. Brain-derived neurotrophic factor in the ventromedial nucleus of the hypothalamus reduces energy intake. Am J Physiol Regul Integr Comp Physiol 293 (2007) R1037-R1045
188. Wang R., Cruciani-Guglielmacci C., Migrenne S., Magnan C., Cotero V.E., and Routh V.H. Effects of oleic acid on distinct populations of neurons in the hypothalamic arcuate nucleus are dependent on extracellular glucose levels. J Neurophysiol 95 (2006) 1491-1498
189. Williams D.L., Kaplan J.M., and Grill H.J. The role of the dorsal vagal complex and the vagus nerve in feeding effects of melanocortin-3/4 receptor stimulation. Endocrinology 141 (2000) 1332-1337
190. Wisse B.E., Kim F., and Schwartz M.W. Physiology. An integrative view of obesity. Science 318 (2007) 928-929
191. Wolfgang M.J., Cha S.H., Sidhaye A., Chohnan S., Cline G., Shulman G.I., et al. Regulation of hypothalamic malonyl-CoA by central glucose and leptin. Proc Natl Acad Sci USA 104 (2007) 19285-19290
192. Wolfgang M.J., Kurama T., Dai Y., Suwa A., Asaumi M., Matsumoto S., et al. The brain-specific carnitine palmitoyltransferase-1c regulates energy homeostasis. Proc Natl Acad Sci USA 103 (2006) 7282-7287
193. Woods S.C. The control of food intake: behavioral versus molecular perspectives. Cell Metab 9 (2009) 489-498
194. Wu X., Gao J., Yan J., Owyang C., and Li Y. Hypothalamus-brain stem circuitry responsible for vagal efferent signalling to the pancreas evoked by hypoglycemia in rat. J Neurophysiol 91 (2004) 1734-1747
195. Xu A.W., Kaelin C.B., Morton G.J., Ogimoto K., Stanhope K., Graham J., et al. Effects of hypothalamic neurodegeneration on energy balance. PLoS Biol 3 (2005) e415
196. Xu B., Goulding E.H., Zang K., Cepoi D., Cone R.D., Jones K.R., et al. Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat Neurosci 6 (2003) 736-742
197. Xu Y., Jones J.E., Kohno D., Williams K.W., Lee C.E., Choi M.J., et al. 5-HT2CRs expressed by pro-opiomelanocortin neurons regulate energy homeostasis. Neuron 60 (2008) 582-589
198. Yamanaka A., Beuckmann C.T., Willie J.T., Hara J., Tsujino N., Mieda M., et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38 (2003) 701-713
199. Yang X.J., Kow L.M., Funabashi T., and Mobbs C.V. Hypothalamic glucose sensor: similarities to and differences from pancreatic beta-cell mechanisms. Diabetes 48 (1999) 1763-1772
200. Yaswen L., Diehl N., Brennan M.B., and Hochgeschwender U. Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin. Nat Med 5 (1999) 1066-1070
201. Yeo G.S., Connie Hung C.C., Rochford J., Keogh J., Gray J., Sivaramakrishnan S., et al. A de novo mutation affecting human TrkB associated with severe obesity and developmental delay. Nat Neurosci 7 (2004) 1187-1189
202. Yi C.X., Serlie M.J., Ackermans M.T., Foppen E., Buijs R.M., Sauerwein H.P., et al. A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58 (2009) 1998-2005
203. Youngstrom T.G., and Bartness T.J. Catecholaminergic innervation of white adipose tissue in Siberian hamsters. Am J Physiol 268 (1995) R744-751
204. Zhang R., Dhillon H., Yin H., Yoshimura A., Lowell B.B., Maratos-Flier E., et al. Selective inactivation of Socs3 in SF1 neurons improves glucose homeostasis without affecting body weight. Endocrinology 149 (2008) 5654-5661
205. Zhang X., Zhang G., Zhang H., Karin M., Bai H., and Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 135 (2008) 61-73
206. Zheng H., Patterson L.M., and Berthoud H.R. Orexin signalling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 27 (2007) 11075-11082
207. Zheng H., Patterson L.M., Morrison C., Banfield B.W., Randall J.A., Browning K.N., et al. Melanin concentrating hormone innervation of caudal brainstem areas involved in gastrointestinal functions and energy balance. Neuroscience 135 (2005) 611-625