Fatty acid sensing in the gut and the hypothalamus: In vivo and in vitro perspectives

Molecular and Cellular Endocrinology

Volumn 397, Issue 1-2, 2014, Pages 23-33

  Duca, Frank A ^a   Yue, Jessica T Y ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Fatty acids; Gut; Hypothalamus

Indexed keywords

FATTY ACID;

ANIMAL; BIOLOGICAL MODEL; CELL LINE; ESTERIFICATION; FOOD INTAKE; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMAN; HYPOTHALAMUS; LIPID METABOLISM; METABOLISM; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION;

ANIMALS; APPETITE REGULATION; CELL LINE; ESTERIFICATION; FATTY ACIDS; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS; HYPOTHALAMUS; LIPID METABOLISM; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION;

EID: 84914120663     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.09.022     Document Type: Review

References (147)

1. Beiroa D., Imbernon M., Gallego R., Senra A., Herranz D., Villaroya F., et al. GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. Diabetes 2014, 10.2337/db14-0302.
2. 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 2009, 119:2577-2589.
3. Bittar P.G., Charnay Y., Pellerin L., Bouras C., Magistretti P.J. Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J. Cereb. Blood Flow Metab 1996, 16:1079-1089.
4. Blazquez C., Sanchez C., Velasco G., Guzman M. Role of carnitine palmitoyltransferase I in the control of ketogenesis in primary cultures of rat astrocytes. J. Neurochem 1998, 71:1597-1606.
5. Blevins J.E., Stanley B.G., Reidelberger R.D. Brain regions where cholecystokinin suppresses feeding in rats. Brain Res 2000, 860:1-10.
6. Boden G., She P., Mozzoli M., Cheung P., Gumireddy K., Reddy P., et al. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappaB pathway in rat liver. Diabetes 2005, 54:3458-3465.
7. Breen D.M., Yue J.T., Rasmussen B.A., Kokorovic A., Cheung G.W., Lam T.K. Duodenal PKC-delta and cholecystokinin signaling axis regulates glucose production. Diabetes 2011, 60:3148-3153.
8. Breen D.M., Rasmussen B.A., Kokorovic A., Wang R., Cheung G.W., Lam T.K. Jejunal nutrient sensing is required for duodenal-jejunal bypass surgery to rapidly lower glucose concentrations in uncontrolled diabetes. Nat. Med 2012, 18:950-955.
9. Broberger C., Holmberg K., Shi T.J., Dockray G., Hokfelt T. Expression and regulation of cholecystokinin and cholecystokinin receptors in rat nodose and dorsal root ganglia. Brain Res 2001, 903:128-140.
10. Brubaker P.L. Regulation of intestinal proglucagon-derived peptide secretion by intestinal regulatory peptides. Endocrinology 1991, 128:3175-3182.
11. Cabou C., Vachoux C., Campistron G., Drucker D.J., Burcelin R. Brain GLP-1 signaling regulates femoral artery blood flow and insulin sensitivity through hypothalamic PKC-{delta}. Diabetes 2011, 60:2245-2256.
12. Campos C.A., Wright J.S., Czaja K., Ritter R.C. CCK-induced reduction of food intake and hindbrain MAPK signaling are mediated by NMDA receptor activation. Endocrinology 2012, 153:2633-2646.
13. Campos C.A., Shiina H., Silvas M., Page S., Ritter R.C. Vagal afferent NMDA receptors modulate CCK-induced reduction of food intake through synapsin I phosphorylation in adult male rats. Endocrinology 2013, 154:2613-2625.
14. Caspi L., Wang P.Y., Lam T.K. A balance of lipid-sensing mechanisms in the brain and liver. Cell Metab 2007, 6:99-104.
15. Cesquini M., Stoppa G.R., Prada P.O., Torsoni A.S., Romanatto T., Souza A., et al. Citrate diminishes hypothalamic acetyl-CoA carboxylase phosphorylation and modulates satiety signals and hepatic mechanisms involved in glucose homeostasis in rats. Life Sci 2008, 82:1262-1271.
16. Cha S.H., Lane M.D. Central lactate metabolism suppresses food intake via the hypothalamic AMP kinase/malonyl-CoA signaling pathway. Biochem. Biophys. Res. Commun 2009, 386:212-216.
17. Champaneria S., Costall B., Naylor R.J., Robertson D.W. Identification and distribution of 5-HT3 recognition sites in the rat gastrointestinal tract. Br. J. Pharmacol 1992, 106:693-696.
18. Chaudhri O.B., Field B.C., Bloom S.R. Gastrointestinal satiety signals. Int. J. Obes 2008, 32(Suppl. 7):S28-S31.
19. Cheung G.W., Kokorovic A., Lam C.K., Chari M., Lam T.K. Intestinal cholecystokinin controls glucose production through a neuronal network. Cell Metab 2009, 10:99-109.
20. Cintra D.E., Ropelle E.R., Moraes J.C., Pauli J.R., Morari J., Souza C.T., et al. Unsaturated fatty acids revert diet-induced hypothalamic inflammation in obesity. PLoS ONE 2012, 7:e30571.
21. Clegg D.J., Gotoh K., Kemp C., Wortman M.D., Benoit S.C., Brown L.M., et al. Consumption of a high-fat diet induces central insulin resistance independent of adiposity. Physiol. Behav 2011, 103:10-16.
22. Contreras C., Gonzalez F., Ferno J., Dieguez C., Rahmouni K., Nogueiras R., et al. The brain and brown fat. Ann. Med 2014, 1-19.
23. Cote C.D., Zadeh-Tahmasebi M., Rasmussen B.A., Duca F.A., Lam T.K. Hormonal signaling in the gut. J. Biol. Chem 2014, 289:11642-11649.
24. Dailey M.J., Moghadam A.A., Moran T.H. Jejunal linoleic acid infusions require GLP-1 receptor signaling to inhibit food intake: implications for the effectiveness of Roux-en-Y gastric bypass. Am. J. Physiol. Endocrinol. Metab 2011, 301:E1184-E1190.
25. Darling R.A., Zhao H., Kinch D., Li A.J., Simasko S.M., Ritter S. Mercaptoacetate and fatty acids exert direct and antagonistic effects on nodose neurons via GPR40 fatty acid receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol 2014, 307:R35-R43.
26. De Souza C.T., Araujo E.P., Bordin S., Ashimine R., Zollner R.L., Boschero A.C., et al. Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus. Endocrinology 2005, 146:4192-4199.
27. Dieguez C., Fruhbeck G., Lopez M. Hypothalamic lipids and the regulation of energy homeostasis. Obes. Facts 2009, 2:126-135.
28. Drucker D.J., Jin T., Asa S.L., Young T.A., Brubaker P.L. Activation of proglucagon gene transcription by protein kinase-A in a novel mouse enteroendocrine cell line. Mol. Endocrinol 1994, 8:1646-1655.
29. Duca F.A., Covasa M. Current and emerging concepts on the role of peripheral signals in the control of food intake and development of obesity. Br. J. Nutr 2012, 108:778-793.
30. Duca F.A., Sakar Y., Covasa M. The modulatory role of high fat feeding on gastrointestinal signals in obesity. J. Nutr. Biochem 2013, 24:1663-1677.
31. Eastwood C., Maubach K., Kirkup A.J., Grundy D. The role of endogenous cholecystokinin in the sensory transduction of luminal nutrient signals in the rat jejunum. Neurosci. Lett 1998, 254:145-148.
32. Edfalk S., Steneberg P., Edlund H. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 2008, 57:2280-2287.
33. Edmond J., Robbins R.A., Bergstrom J.D., Cole R.A., de Vellis J. Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes, and oligodendrocytes from developing brain in primary culture. J. Neurosci. Res 1987, 18:551-561.
34. Freed L.M., Wakabayashi S., Bell J.M., Rapoport S.I. Effect of inhibition of beta-oxidation on incorporation of [U-14C]palmitate and [1-14C]arachidonate into brain lipids. Brain Res 1994, 645:41-48.
35. Gao S., Keung W., Serra D., Wang W., Carrasco P., Casals N., et al. Malonyl-CoA mediates leptin hypothalamic control of feeding independent of inhibition of CPT-1a. Am. J. Physiol. Regul. Integr. Comp. Physiol 2011, 301:R209-R217.
36. Gao S., Zhu G., Gao X., Wu D., Carrasco P., Casals N., et al. Important roles of brain-specific carnitine palmitoyltransferase and ceramide metabolism in leptin hypothalamic control of feeding. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9691-9696.
37. Greco J.A., Oosterman J.E., Belsham D.D. Differential effects of omega-3 fatty acid DHA and palmitate on the circadian transcriptional profile of clock genes in immortalized hypothalamic neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol 2014, PMID: 25144192.
38. Greenberg D., Smith G.P., Gibbs J. Intraduodenal infusions of fats elicit satiety in sham-feeding rats. Am. J. Physiol 1990, 259:R110-R118.
39. Guzman M., Blazquez C. Is there an astrocyte-neuron ketone body shuttle?. Trends Endocrinol. Metab 2001, 12:169-173.
40. Habib A.M., Richards P., Cairns L.S., Rogers G.J., Bannon C.A., Parker H.E., et al. Overlap of endocrine hormone expression in the mouse intestine revealed by transcriptional profiling and flow cytometry. Endocrinology 2012, 153:3054-3065.
41. Hamilton J.A., Brunaldi K. A model for fatty acid transport into the brain. J. Mol. Neurosci 2007, 33:12-17.
42. Hayes M.R., Covasa M. CCK and 5-HT act synergistically to suppress food intake through simultaneous activation of CCK-1 and 5-HT3 receptors. Peptides 2005, 26:2322-2330.
43. Hayes M.R., Covasa M. Dorsal hindbrain 5-HT3 receptors participate in control of meal size and mediate CCK-induced satiation. Brain Res 2006, 1103:99-107.
44. Hayes M.R., Covasa M. Gastric distension enhances CCK-induced Fos-like immunoreactivity in the dorsal hindbrain by activating 5-HT3 receptors. Brain Res 2006, 1088:120-130.
45. Hayes M.R., Chory F.M., Gallagher C.A., Covasa M. Serotonin type-3 receptors mediate cholecystokinin-induced satiation through gastric distension. Am. J. Physiol. Regul. Integr. Comp. Physiol 2006, 291:R115-R123.
46. He W., Lam T.K., Obici S., Rossetti L. Molecular disruption of hypothalamic nutrient sensing induces obesity. Nat. Neurosci 2006, 9:227-233.
47. Hirasawa A., Tsumaya K., Awaji T., Katsuma S., Adachi T., Yamada M., et al. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat. Med 2005, 11:90-94.
48. Holland W.L., Bikman B.T., Wang L.P., Yuguang G., Sargent K.M., Bulchand S., et al. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest 2011, 121:1858-1870.
49. Hu Z., Dai Y., Prentki M., Chohnan S., Lane M.D. A role for hypothalamic malonyl-CoA in the control of food intake. J. Biol. Chem 2005, 280:39681-39683.
50. Iakoubov R., Izzo A., Yeung A., Whiteside C.I., Brubaker P.L. Protein kinase Czeta is required for oleic acid-induced secretion of glucagon-like peptide-1 by intestinal endocrine L cells. Endocrinology 2007, 148:1089-1098.
51. Iakoubov R., Ahmed A., Lauffer L.M., Bazinet R.P., Brubaker P.L. Essential role for protein kinase Czeta in oleic acid-induced glucagon-like peptide-1 secretion in vivo in the rat. Endocrinology 2011, 152:1244-1252.
52. Ichimura A., Hirasawa A., Poulain-Godefroy O., Bonnefond A., Hara T., Yengo L., et al. Dysfunction of lipid sensor GPR120 leads to obesity in both mouse and human. Nature 2012, 483:350-354.
53. Janssen S., Depoortere I. Nutrient sensing in the gut: new roads to therapeutics?. Trends Endocrinol. Metab 2013, 24:92-100.
54. Jo Y.H., Su Y., Gutierrez-Juarez R., Chua S. Oleic acid directly regulates POMC neuron excitability in the hypothalamus. J. Neurophysiol 2009, 101:2305-2316.
55. Karaki S., Mitsui R., Hayashi H., Kato I., Sugiya H., Iwanaga T., et al. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res 2006, 353-360.
56. Kim M.S., Park J.Y., Namkoong C., Jang P.G., Ryu J.W., Song H.S., et al. Anti-obesity effects of alpha-lipoic acid mediated by suppression of hypothalamic AMP-activated protein kinase. Nat. Med 2004, 10:727-733.
57. Kleinridders A., Schenten D., Konner A.C., Belgardt B.F., Mauer J., Okamura T., et al. MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity. Cell Metab 2009, 10:249-259.
58. Kokorovic A., Cheung G.W., Breen D.M., Chari M., Lam C.K., Lam T.K. Duodenal mucosal protein kinase C-delta regulates glucose production in rats. Gastroenterology 2011, 141:1720-1727.
59. Kola B., Hubina E., Tucci S.A., Kirkham T.C., Garcia E.A., Mitchell S.E., et al. Cannabinoids and ghrelin have both central and peripheral metabolic and cardiac effects via AMP-activated protein kinase. J. Biol. Chem 2005, 280:25196-25201.
60. Kubota N., Yano W., Kubota T., Yamauchi T., Itoh S., Kumagai H., et al. Adiponectin stimulates AMP-activated protein kinase in the hypothalamus and increases food intake. Cell Metab 2007, 6:55-68.
61. Kuo D.Y., Yang S.F., Chu S.C., Chu S.C., Chen C.H., Hsieh Y.S. Amphetamine-evoked changes of oxidative stress and neuropeptide Y gene expression in hypothalamus: regulation by the protein kinase C-delta signaling. Chem. Biol. Interact 2009, 180:193-201.
62. Lage R., Dieguez C., Vidal-Puig A., Lopez M. AMPK: a metabolic gauge regulating whole-body energy homeostasis. Trends Mol. Med 2008, 14:539-549.
63. Lal S., Kirkup A.J., Brunsden A.M., Thompson D.G., Grundy D. Vagal afferent responses to fatty acids of different chain length in the rat. Am. J. Physiol. Gastrointest. Liver Physiol 2001, 281:G907-G915.
64. Lam C.K., Chari M., Wang P.Y., Lam T.K. Central lactate metabolism regulates food intake. Am. J. Physiol. Endocrinol. Metab 2008, 295:E491-E496.
65. Lam C.K., Chari M., Lam T.K. CNS regulation of glucose homeostasis. Physiology (Bethesda) 2009, 24:159-170.
66. Lam T.K., Yoshii H., Haber C.A., Bogdanovic E., Lam L., Fantus I.G., et al. Free fatty acid-induced hepatic insulin resistance: a potential role for protein kinase C-delta. Am. J. Physiol. Endocrinol. Metab 2002, 283:E682-E691.
67. Lam T.K., Gutierrez-Juarez R., Pocai A., Rossetti L. Regulation of blood glucose by hypothalamic pyruvate metabolism. Science 2005, 309:943-947.
68. 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 2005, 11:320-327.
69. Lam T.K., Schwartz G.J., Rossetti L. Hypothalamic sensing of fatty acids. Nat. Neurosci 2005, 8:579-584.
70. Lan H., Vassileva G., Corona A., Liu L., Baker H., Golovko A., et al. GPR119 is required for physiological regulation of glucagon-like peptide-1 secretion but not for metabolic homeostasis. J. Endocrinol 2009, 201:219-230.
71. Lane M.D., Wolfgang M., Cha S.H., Dai Y. Regulation of food intake and energy expenditure by hypothalamic malonyl-CoA. Int. J. Obes. (Lond) 2008, 32(Suppl. 4):S49-S54.
72. LaPierre M.P., Abraham M.A., Filippi B.M., Yue J.T., Lam T.K. Glucagon and lipid signaling in the hypothalamus. Mamm. Genome 2014, 25:434-441.
73. Le Foll C., Irani B.G., Magnan C., Dunn-Meynell A.A., Levin B.E. Characteristics and mechanisms of hypothalamic neuronal fatty acid sensing. Am. J. Physiol. Regul. Integr. Comp. Physiol 2009, 297:R655-R664.
74. Light P.E., Bladen C., Winkfein R.J., Walsh M.P., French R.J. Molecular basis of protein kinase C-induced activation of ATP-sensitive potassium channels. Proc. Natl Acad. Sci. U.S.A. 2000, 97:9058-9063.
75. Liou A.P., Lu X., Sei Y., Zhao X., Pechhold S., Carrero R.J., et al. The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 2011, 140:903-912.
76. Lopes-Cardozo M., Larsson O.M., Schousboe A. Acetoacetate and glucose as lipid precursors and energy substrates in primary cultures of astrocytes and neurons from mouse cerebral cortex. J. Neurochem 1986, 46:773-778.
77. Lopez M., Tovar S., Vazquez M.J., Nogueiras R., Senaris R., Dieguez C. Sensing the fat: fatty acid metabolism in the hypothalamus and the melanocortin system. Peptides 2005, 26:1753-1758.
78. Lopez M., Varela L., Vazquez M.J., Rodriguez-Cuenca S., Gonzalez C.R., Velagapudi V.R., et al. Hypothalamic AMPK and fatty acid metabolism mediate thyroid regulation of energy balance. Nat. Med 2010, 16:1001-1008.
79. Magistretti P.J., Sorg O., Yu N., Martin J.L., Pellerin L. Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev. Neurosci 1993, 15:306-312.
80. Magistretti P.J., Pellerin L., Rothman D.L., Shulman R.G. Energy on demand. Science 1999, 283:496-497.
81. Maljaars P.W., Peters H.P., Mela D.J., Masclee A.A. Ileal brake: a sensible food target for appetite control. A review. Physiol. Behav 2008, 95:271-281.
82. Maljaars P.W., Peters H.P., Kodde A., Geraedts M., Troost F.J., Haddeman E., et al. Length and site of the small intestine exposed to fat influences hunger and food intake. Br. J. Nutr 2011, 106:1609-1615.
83. Martinez de Morentin P.B., Whittle A.J., Ferno J., Nogueiras R., Dieguez C., Vidal-Puig A., et al. Nicotine induces negative energy balance through hypothalamic AMP-activated protein kinase. Diabetes 2012, 61:807-817.
84. Martinez de Morentin P.B., Gonzalez-Garcia I., Martins L., Lage R., Fernandez-Mallo D., Martinez-Sanchez N., et al. Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. Cell Metab 2014, 20:41-53.
85. Mayer C.M., Belsham D.D. Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 5' monophosphate-activated protein kinase activation. Endocrinology 2010, 151:576-585.
86. McGarry J.D., Mannaerts G.P., Foster D.W. A possible role for malonyl-CoA in the regulation of hepatic fatty acid oxidation and ketogenesis. J. Clin. Invest 1977, 60:265-270.
87. McGarry J.D., Mills S.E., Long C.S., Foster D.W. Observations on the affinity for carnitine, and malonyl-CoA sensitivity, of carnitine palmitoyltransferase I in animal and human tissues. Demonstration of the presence of malonyl-CoA in non-hepatic tissues of the rat. Biochem. J. 1983, 214:21-28.
88. McLaughlin J.T., Lomax R.B., Hall L., Dockray G.J., Thompson D.G., Warhurst G. Fatty acids stimulate cholecystokinin secretion via an acyl chain length-specific, Ca2+-dependent mechanism in the enteroendocrine cell line STC-1. J. Physiol 1998, 513:11-18.
89. Miller J.C., Gnaedinger J.M., Rapoport S.I. Utilization of plasma fatty acid in rat brain: distribution of [14C]palmitate between oxidative and synthetic pathways. J. Neurochem 1987, 49:1507-1514.
90. 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 2004, 428:569-574.
91. Mitchell R.W., Edmundson C.L., Miller D.W., Hatch G.M. On the mechanism of oleate transport across human brain microvessel endothelial cells. J. Neurochem 2009, 110:1049-1057.
92. Monnikes H., Lauer G., Bauer C., Tebbe J., Zittel T.T., Arnold R. Pathways of Fos expression in locus ceruleus, dorsal vagal complex, and PVN in response to intestinal lipid. Am. J. Physiol 1997, 273:R2059-R2071.
93. Morgan K., Obici S., Rossetti L. Hypothalamic responses to long-chain fatty acids are nutritionally regulated. J. Biol. Chem 2004, 279:31139-31148.
94. Moulle V.S., Le F.C., Philippe E., Kassis N., Rouch C., Marsollier N., et al. Fatty acid transporter CD36 mediates hypothalamic effect of fatty acids on food intake in rats. PLoS ONE 2013, 8:e74021.
95. Moulle V.S., Picard A., Le F.C., Levin B.E., Magnan C. Lipid sensing in the brain and regulation of energy balance. Diabetes Metab 2014, 40:29-33.
96. Obici S., Feng Z., Morgan K., Stein D., Karkanias G., Rossetti L. Central administration of oleic acid inhibits glucose production and food intake. Diabetes 2002, 51:271-275.
97. Obici S., Feng Z., Arduini A., Conti R., Rossetti L. Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat. Med 2003, 9:756-761.
98. Oh D.Y., Talukdar S., Bae E.J., Imamura T., Morinaga H., Fan W., et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010, 142:687-698.
99. Oh D.Y., Walenta E., Akiyama T.E., Lagakos W.S., Lackey D., Pessentheiner A.R., et al. A Gpr120-selective agonist improves insulin resistance and chronic inflammation in obese mice. Nat. Med 2014, 20:942-947.
100. Oomura Y., Nakamura T., Sugimori M., Yamada Y. Effect of free fatty acid on the rat lateral hypothalamic neurons. Physiol. Behav 1975, 14:483-486.
101. Pardridge W.M., Oldendorf W.H. Transport of metabolic substrates through the blood-brain barrier. J. Neurochem 1977, 28:5-12.
102. Pellerin L. Food for thought: the importance of glucose and other energy substrates for sustaining brain function under varying levels of activity. Diabetes Metab 2010, 36(Suppl. 3):S59-S63.
103. Picard A., Rouch C., Kassis N., Moulle V.S., Croizier S., Denis R.G., et al. Hippocampal lipoprotein lipase regulates energy balance in rodents. Mol. Metab 2014, 3:167-176.
104. 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 2005, 434:1026-1031.
105. Poreba M.A., Dong C.X., Li S.K., Stahl A., Miner J.H., Brubaker P.L. Role of fatty acid transport protein 4 in oleic acid-induced glucagon-like peptide-1 secretion from murine intestinal L cells. Am. J. Physiol. Endocrinol. Metab 2012, 303:E899-E907.
106. Powley T.L., Spaulding R.A., Haglof S.A. Vagal afferent innervation of the proximal gastrointestinal tract mucosa: chemoreceptor and mechanoreceptor architecture. J. Comp. Neurol 2011, 519:644-660.
107. Price N., van der Leij F., Jackson V., Corstorphine C., Thomson R., Sorensen A., et al. A novel brain-expressed protein related to carnitine palmitoyltransferase I. Genomics 2002, 80:433-442.
108. Prpic V., Basavappa S., Liddle R.A., Mangel A.W. Regulation of cholecystokinin secretion by calcium-dependent calmodulin kinase II: differential effects of phenylalanine and cAMP. Biochem. Biophys. Res. Commun 1994, 201:1483-1489.
109. Ramirez S., Martins L., Jacas J., Carrasco P., Pozo M., Clotet J., et al. Hypothalamic ceramide levels regulated by CPT1C mediate the orexigenic effect of ghrelin. Diabetes 2013, 62:2329-2337.
110. Randich A., Tyler W.J., Cox J.E., Meller S.T., Kelm G.R., Bharaj S.S. Responses of celiac and cervical vagal afferents to infusions of lipids in the jejunum or ileum of the rat. Am. J. Physiol-Reg. I. 2000, 278:R34-R43.
111. Rasmussen B.A., Breen D.M., Luo P., Cheung G.W., Yang C.S., Sun B., et al. Duodenal activation of cAMP-dependent protein kinase induces vagal afferent firing and lowers glucose production in rats. Gastroenterology 2012, 142:834-843.
112. Rasmussen B.A., Breen D.M., Duca F.A., Cote C.D., Zadeh-Tahmasebi M., Filippi B.M., et al. Jejunal leptin-PI3K signaling lowers glucose production. Cell Metab 2014, 19:155-161.
113. Reimann F., Habib A.M., Tolhurst G., Parker H.E., Rogers G.J., Gribble F.M. Glucose sensing in L cells: a primary cell study. Cell Metab 2008, 8:532-539.
114. Reimer R.A., Darimont C., Gremlich S., Nicolas-Metral V., Ruegg U.T., Mace K. A human cellular model for studying the regulation of glucagon-like peptide-1 secretion. Endocrinology 2001, 142:4522-4528.
115. Rindi G., Grant S.G., Yiangou Y., Ghatei M.A., Bloom S.R., Bautch V.L., et al. Development of neuroendocrine tumors in the gastrointestinal tract of transgenic mice. Heterogeneity of hormone expression. Am. J. Pathol 1990, 136:1349-1363.
116. Ritter R.C. Gastrointestinal mechanisms of satiation for food. Physiol. Behav 2004, 81:249-273.
117. Ritter R.C. A tale of two endings: modulation of satiation by NMDA receptors on or near central and peripheral vagal afferent terminals. Physiol. Behav 2011, 105:94-99.
118. Rogers R.C., Hermann G.E. Mechanisms of action of CCK to activate central vagal afferent terminals. Peptides 2008, 29:1716-1725.
119. Ross R., Wang P.Y., Chari M., Lam C.K., Caspi L., Ono H., et al. Hypothalamic protein kinase C regulates glucose production. Diabetes 2008, 57:2061-2065.
120. Samuel V.T., Liu Z.X., Qu X., Elder B.D., Bilz S., Befroy D., et al. Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J. Biol. Chem 2004, 279:32345-32353.
121. Sandoval D.A., Bagnol D., Woods S.C., D'Alessio D.A., Seeley R.J. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008, 57:2046-2054.
122. Schwartz G.J., Fu J., Astarita G., Li X., Gaetani S., Campolongo P., et al. The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 2008, 8:281-288.
123. Sclafani A., Ackroff K., Schwartz G.J. Selective effects of vagal deafferentation and celiac-superior mesenteric ganglionectomy on the reinforcing and satiating action of intestinal nutrients. Physiol. Behav 2003, 78:285-294.
124. Scott L., Prpic V., Capel W.D., Basavappa S., Mangel A.W., Gettys T.W., et al. Beta-adrenergic regulation of cholecystokinin secretion in STC-1 cells. Am. J. Physiol 1996, 270:G291-G297.
125. Shah B.P., Liu P., Yu T., Hansen D.R., Gilbertson T.A. TRPM5 is critical for linoleic acid-induced CCK secretion from the enteroendocrine cell line, STC-1. Am. J. Physiol. Cell Physiol 2012, 302:C210-C219.
126. Shulman G.I. Cellular mechanisms of insulin resistance. J. Clin. Invest 2000, 106:171-176.
127. Sidhu S.S., Thompson D.G., Warhurst G., Case R.M., Benson R.S. Fatty acid-induced cholecystokinin secretion and changes in intracellular Ca2+ in two enteroendocrine cell lines, STC-1 and GLUTag. J. Physiol 2000, 528(Pt 1):165-176.
128. Sundaresan S., Shahid R., Riehl T.E., Chandra R., Nassir F., Stenson W.F., et al. CD36-dependent signaling mediates fatty acid-induced gut release of secretin and cholecystokinin. FASEB J. 2013, 27:1191-1202.
129. Sutton G.M., Patterson L.M., Berthoud H.R. Extracellular signal-regulated kinase 1/2 signaling pathway in solitary nucleus mediates cholecystokinin-induced suppression of food intake in rats. J. Neurosci 2004, 24:10240-10247.
130. Sykaras A.G., Demenis C., Cheng L., Pisitkun T., McLaughlin J.T., Fenton R.A., et al. Duodenal CCK cells from male mice express multiple hormones including ghrelin. Endocrinology 2014, 155:3339-3351. 10.1210/en.2013-2165.
131. Taib B., Bouyakdan K., Hryhorczuk C., Rodaros D., Fulton S., Alquier T. Glucose regulates hypothalamic long-chain fatty acid metabolism via AMP-activated kinase (AMPK) in neurons and astrocytes. J. Biol. Chem 2013, 288:37216-37229.
132. Tamura C.S., Ritter R.C. Intestinal capsaicin transiently attenuates suppression of sham feeding by oleate. Am. J. Physiol 1994, 267:R561-R568.
133. Tanaka T., Katsuma S., Adachi T., Koshimizu T.A., Hirasawa A., Tsujimoto G. Free fatty acids induce cholecystokinin secretion through GPR120. Naunyn Schmiedebergs Arch. Pharmacol 2008, 377:523-527.
134. Wang H., Astarita G., Taussig M.D., Bharadwaj K.G., DiPatrizio N.V., Nave K.A., et al. Deficiency of lipoprotein lipase in neurons modifies the regulation of energy balance and leads to obesity. Cell Metab 2011, 13:105-113.
135. Wang P.Y., Caspi L., Lam C.K., Chari M., Li X., Light P.E., et al. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 2008, 452:1012-1016.
136. Wang R., Cruciani-Guglielmacci C., Migrenne S., Magnan C., Cotero V.E., 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 2006, 95:1491-1498.
137. Webster W.A., Beyak M.J. The long chain fatty acid oleate activates mouse intestinal afferent nerves in vitro. Can. J. Physiol. Pharmacol 2013, 91:375-379.
138. Wellhauser L., Belsham D.D. Activation of the omega-3 fatty acid receptor GPR120 mediates anti-inflammatory actions in immortalized hypothalamic neurons. J. Neuroinflammation 2014, 11:60.
139. Wolfgang M.J., Lane M.D. Hypothalamic malonyl-CoA and CPT1c in the treatment of obesity. FEBS J. 2011, 278:552-558.
140. 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. U.S.A. 2006, 103:7282-7287.
141. Xiong Y., Swaminath G., Cao Q., Yang L., Guo Q., Salomonis H., et al. Activation of FFA1 mediates GLP-1 secretion in mice. Evidence for allosterism at FFA1. Mol. Cell. Endocrinol 2013, 369:119-129.
142. Yang C.S., Lam C.K., Chari M., Cheung G.W., Kokorovic A., Gao S., et al. Hypothalamic AMP-activated protein kinase regulates glucose production. Diabetes 2010, 59:2435-2443.
143. Yang G., Badeanlou L., Bielawski J., Roberts A.J., Hannun Y.A., Samad F. Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am. J. Physiol. Endocrinol. Metab 2009, 297:E211-E224.
144. Yi C.X., Habegger K.M., Chowen J.A., Stern J., Tschop M.H. A role for astrocytes in the central control of metabolism. Neuroendocrinology 2011, 93:143-149.
145. Yox D.P., Brenner L., Ritter R.C. CCK-receptor antagonists attenuate suppression of sham feeding by intestinal nutrients. Am. J. Physiol 1992, 262:R554-R561.
146. Yue J.T., Lam T.K. Lipid sensing and insulin resistance in the brain. Cell Metab 2012, 15:646-655.
147. Zhang X., Zhang G., Zhang H., Karin M., Bai H., Cai D. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 2008, 135:61-73.