Brainstem nutrient sensing in the nucleus of the solitary tract inhibits feeding

Cell Metabolism

Volumn 16, Issue 5, 2012, Pages 579-587

  Blouet, Clemence ^a   Schwartz, Gary J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE; PROTEIN P70; PROTEIN S6; S6 KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; BRAIN STEM; CONTROLLED STUDY; ENERGY BALANCE; FEEDING; FOOD INTAKE; FOREBRAIN; IMMUNOREACTIVITY; INHIBITION KINETICS; MEAL; NONHUMAN; NUTRIENT AVAILABILITY; NUTRITIONAL STATUS; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS;

RATTUS;

EID: 84871405563     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.10.003     Document Type: Article

References (58)

1. Azzara, A.V., Sokolnicki, J.P., and Schwartz, G.J. (2002). Central melanocortin receptor agonist reduces spontaneous and scheduled meal size but does not augment duodenal preload-induced feeding inhibition. Physiol. Behav. 77, 411-416.
2. Babic, T., Townsend, R.L., Patterson, L.M., Sutton, G.M., Zheng, H., and Berthoud, H.R. (2009). Phenotype of neurons in the nucleus of the solitary tract that express CCK-induced activation of the ERK signaling pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R845-R854.
3. Balfour, R.H., and Trapp, S. (2007). Ionic currents underlying the response of rat dorsal vagal neurones to hypoglycaemia and chemical anoxia. J. Physiol. 579, 691-702.
4. Blevins, J.E., Schwartz, M.W., and Baskin, D.G. (2004). 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, R87-R96.
5. Blevins, J.E., Morton, G.J., Williams, D.L., Caldwell, D.W., Bastian, L.S., Wisse, B.E., Schwartz, M.W., and Baskin, D.G. (2009). Forebrain melanocortin signaling enhances the hindbrain satiety response to CCK-8. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R476-R484.
6. Blouet, C., Ono, H., and Schwartz, G.J. (2008). Mediobasal hypothalamic p70 S6 kinase 1 modulates the control of energy homeostasis. Cell Metab. 8, 459-467.
7. Blouet, C., Jo, Y.H., Li, X., and Schwartz, G.J. (2009). Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus- brainstem circuit. J. Neurosci. 29, 8302-8311.
8. Campos, C.A., Wright, J.S., Czaja, K., and Ritter, R.C. (2012). CCK-induced reduction of food intake and hindbrain MAPK signaling are mediated by NMDA receptor activation. Endocrinology 153, 2633-2646.
9. Cota, D., Proulx, K., Smith, K.A., Kozma, S.C., Thomas, G., Woods, S.C., and Seeley, R.J. (2006). Hypothalamic mTOR signaling regulates food intake. Science 312, 927-930.
10. Cui, R.J., Li, X., and Appleyard, S.M. (2011). Ghrelin inhibits visceral afferent activation of catecholamine neurons in the solitary tract nucleus. J. Neurosci. 31, 3484-3492.
11. Dagon, Y., Hur, E., Zheng, B., Wellenstein, K., Cantley, L.C., and Kahn, B.B. (2012). p70S6 kinase phosphorylates AMPK on serine 491 to mediate leptin's effect on food intake. Cell Metab. 16, 104-112.
12. Daniels, D., Patten, C.S., Roth, J.D., Yee, D.K., and Fluharty, S.J. (2003). Melanocortin receptor signaling through mitogen-activated protein kinase in vitro and in rat hypothalamus. Brain Res. 986, 1-11.
13. Dickson, S.L., Shirazi, R.H., Hansson, C., Bergquist, F., Nissbrandt, H., and Skibicka, K.P. (2012). The glucagon-like peptide 1 (GLP-1) analogue, exendin- 4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J. Neurosci. 32, 4812-4820.
14. Emond, M., Schwartz, G.J., Ladenheim, E.E., and Moran, T.H. (1999). Central leptin modulates behavioral and neural responsivity to CCK. Am. J. Physiol. 276, R1545-R1549.
15. Fan, W., Ellacott, K.L., Halatchev, I.G., Takahashi, K., Yu, P., and Cone, R.D. (2004). Cholecystokinin-mediated suppression of feeding involves the brainstem melanocortin system. Nat. Neurosci. 7, 335-336.
16. Faulconbridge, L.F., Cummings, D.E., Kaplan, J.M., and Grill, H.J. (2003). Hyperphagic effects of brainstem ghrelin administration. Diabetes 52, 2260-2265.
17. González-Mejia, M.E., Morales, M., Hernández-Kelly, L.C., Zepeda, R.C., Bernabé, A., and Ortega, A. (2006). Glutamate-dependent translational regulation in cultured Bergmann glia cells: involvement of p70S6K. Neuroscience 141, 1389-1398.
18. Grill, H.J. (2006). Distributed neural control of energy balance: contributions from hindbrain and hypothalamus. Obesity (Silver Spring) 14(Suppl 5), 216S-221S.
19. Grill, H.J., and Hayes, M.R. (2009). The nucleus tractus solitarius: a portal for visceral afferent signal processing, energy status assessment and integration of their combined effects on food intake. Int J Obes (Lond) 33(Suppl 1), S11-S15.
20. Grill, H.J., Schwartz, M.W., Kaplan, J.M., Foxhall, J.S., Breininger, J., and Baskin, D.G. (2002). Evidence that the caudal brainstem is a target for the inhibitory effect of leptin on food intake. Endocrinology 143, 239-246.
21. Hardie, D.G., Ross, F.A., and Hawley, S.A. (2012). AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251-262.
22. Hayes, M.R., Bradley, L., and Grill, H.J. (2009). Endogenous hindbrain glucagon-like peptide-1 receptor activation contributes to the control of food intake by mediating gastric satiation signaling. Endocrinology 150, 2654-2659.
23. Hayes, M.R., Skibicka, K.P., Leichner, T.M., Guarnieri, D.J., DiLeone, R.J., Bence, K.K., and Grill, H.J. (2010). Endogenous leptin signaling in the caudal nucleus tractus solitarius and area postrema is required for energy balance regulation. Cell Metab. 11, 77-83.
24. Hayes, M.R., Leichner, T.M., Zhao, S., Lee, G.S., Chowansky, A., Zimmer, D., De Jonghe, B.C., Kanoski, S.E., Grill, H.J., and Bence, K.K. (2011). Intracellular signals mediating the food intake-suppressive effects of hindbrain glucagonlike peptide-1 receptor activation. Cell Metab. 13, 320-330.
25. Hommel, J.D., Trinko, R., Sears, R.M., Georgescu, D., Liu, Z.W., Gao, X.B., Thurmon, J.J., Marinelli, M., and DiLeone, R.J. (2006). Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51, 801-810.
26. Huo, L., Maeng, L., Bjørbaek, C., and Grill, H.J. (2007). Leptin and the control of food intake: neurons in the nucleus of the solitary tract are activated by both gastric distension and leptin. Endocrinology 148, 2189-2197.
27. Ibrahim, N., Bosch, M.A., Smart, J.L., Qiu, J., Rubinstein, M., Rønnekleiv, O.K., Low, M.J., and Kelly, M.J. (2003). Hypothalamic proopiomelanocortin neurons are glucose responsive and express K(ATP) channels. Endocrinology 144, 1331-1340.
28. Inoki, K., Zhu, T., and Guan, K.L. (2003). TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590.
29. Jo, Y.H., Su, Y., Gutierrez-Juarez, R., and Chua, S., Jr. (2009). Oleic acid directly regulates POMC neuron excitability in the hypothalamus. J. Neurophysiol. 101, 2305-2316.
30. Jordan, S.D., Könner, A.C., and Brüning, J.C. (2010). Sensing the fuels: glucose and lipid signaling in the CNS controlling energy homeostasis. Cell. Mol. Life Sci. 67, 3255-3273.
31. Könner, A.C., Klöckener, T., and Brüning, J.C. (2009). Control of energy homeostasis by insulin and leptin: targeting the arcuate nucleus and beyond. Physiol. Behav. 97, 632-638.
32. Lenz, G., and Avruch, J. (2005). Glutamatergic regulation of the p70S6 kinase in primary mouse neurons. J. Biol. Chem. 280, 38121-38124.
33. Levin, B.E. (2006). Metabolic sensing neurons and the control of energy homeostasis. Physiol. Behav. 89, 486-489.
34. Levin, B.E., Magnan, C., Dunn-Meynell, A., and Le Foll, C. (2011). Metabolic sensing and the brain: who, what, where, and how? Endocrinology 152, 2552-2557.
35. Moran, T.H. (2006). Gut peptide signaling in the controls of food intake. Obesity (Silver Spring) 14(Suppl 5), 250S-253S.
36. Nogueiras, R., Tschöp, M.H., and Zigman, J.M. (2008). Central nervous system regulation of energy metabolism: ghrelin versus leptin. Ann. N Y Acad. Sci. 1126, 14-19.
37. Obici, S., Feng, Z., Morgan, K., Stein, D., Karkanias, G., and Rossetti, L. (2002). Central administration of oleic acid inhibits glucose production and food intake. Diabetes 51, 271-275.
38. Ono, H., Shimano, H., Katagiri, H., Yahagi, N., Sakoda, H., Onishi, Y., Anai, M., Ogihara, T., Fujishiro, M., Viana, A.Y., et al. (2003). Hepatic Akt activation induces marked hypoglycemia, hepatomegaly, and hypertriglyceridemia with sterol regulatory element binding protein involvement. Diabetes 52, 2905-2913.
39. Paxinos, G., and Watson, C. (2001). The Rat Brain in Stereotaxic Coordinates, Fifth Edition (New York: Academic Press).
40. Proud, C.G. (2004). mTOR-mediated regulation of translation factors by amino acids. Biochem. Biophys. Res. Commun. 313, 429-436.
41. Rinaman, L. (2003). Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. J. Neurosci. 23, 10084-10092.
42. Rinaman, L. (2011). Hindbrain noradrenergic A2 neurons: diverse roles in autonomic, endocrine, cognitive, and behavioral functions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R222-R235.
43. Rinaman, L., Verbalis, J.G., Stricker, E.M., and Hoffman, G.E. (1993). Distribution and neurochemical phenotypes of caudal medullary neurons activated to express cFos following peripheral administration of cholecystokinin. J. Comp. Neurol. 338, 475-490.
44. Ritter, S., Dinh, T.T., and Zhang, Y. (2000). Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res. 856, 37-47.
45. Ropelle, E.R., Pauli, J.R., Fernandes, M.F., Rocco, S.A., Marin, R.M., Morari, J., Souza, K.K., Dias, M.M., Gomes-Marcondes, M.C., Gontijo, J.A., et al. (2008). A central role for neuronal AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) in high-protein diet-induced weight loss. Diabetes 57, 594-605.
46. Sanders, N.M., Dunn-Meynell, A.A., and Levin, B.E. (2004). Third ventricular alloxan reversibly impairs glucose counterregulatory responses. Diabetes 53, 1230-1236.
47. Schwartz, G.J., and Moran, T.H. (2002). Leptin and neuropeptide y have opposing modulatory effects on nucleus of the solitary tract neurophysiological responses to gastric loads: implications for the control of food intake. Endocrinology 143, 3779-3784.
48. Schwartz, M.W., Woods, S.C., Porte, D., Jr., Seeley, R.J., and Baskin, D.G. (2000). Central nervous system control of food intake. Nature 404, 661-671.
49. Skibicka, K.P., Hansson, C., Alvarez-Crespo, M., Friberg, P.A., and Dickson, S.L. (2011). Ghrelin directly targets the ventral tegmental area to increase food motivation. Neuroscience 180, 129-137.
50. Smith, G.P. (1996). The direct and indirect controls of meal size. Neurosci. Biobehav. Rev. 20, 41-46.
51. Sutton, G.M., Patterson, L.M., and Berthoud, H.R. (2004). Extracellular signal-regulated kinase 1/2 signaling pathway in solitary nucleus mediates cholecystokinin-induced suppression of food intake in rats. J. Neurosci. 24, 10240-10247.
52. Sutton, G.M., Duos, B., Patterson, L.M., and Berthoud, H.R. (2005). Melanocortinergic modulation of cholecystokinin-induced suppression of feeding through extracellular signal-regulated kinase signaling in rat solitary nucleus. Endocrinology 146, 3739-3747.
53. Wan, S., Browning, K.N., Coleman, F.H., Sutton, G., Zheng, H., Butler, A., Berthoud, H.R., and Travagli, R.A. (2008). Presynaptic melanocortin-4 receptors on vagal afferent fibers modulate the excitability of rat nucleus tractus solitarius neurons. J. Neurosci. 28, 4957-4966.
54. Wang, R., Liu, X., Hentges, S.T., Dunn-Meynell, A.A., Levin, B.E., Wang, W., and Routh, V.H. (2004). The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. Diabetes 53, 1959-1965.
55. Woods, S.C. (2009). The control of food intake: behavioral versus molecular perspectives. Cell Metab. 9, 489-498.
56. Woods, S.C., Seeley, R.J., and Cota, D. (2008). Regulation of food intake through hypothalamic signaling networks involving mTOR. Annu. Rev. Nutr. 28, 295-311.
57. Zhang, Y., Rodrigues, E., Gao, Y.X., King, M., Cheng, K.Y., Erdös, B., Tümer, N., Carter, C., and Scarpace, P.J. (2010). Pro-opiomelanocortin gene transfer to the nucleus of the solitary track but not arcuate nucleus ameliorates chronic diet-induced obesity. Neuroscience 169, 1662-1671.
58. Zhao, S., Kanoski, S.E., Yan, J., Grill, H.J., and Hayes, M.R. (2012). Hindbrain leptin and glucagon-like-peptide-1 receptor signaling interact to suppress food intake in an additive manner. Int J Obes (Lond), in press. Published online January 17, 2012. http://dx.doi.org/10.1038/ijo.2011.265.