Mercaptoacetate and fatty acids exert direct and antagonistic effects on nodose neurons via GPR40 fatty acid receptors

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 1, 2014, Pages

  Darling, Rebecca A ^a   Zhao, Huan ^a   Kinch, Dallas ^a   Li, Ai Jun ^a   Simasko, Steven M ^a   Ritter, Sue ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Calcium imaging; Fatty acids; G protein coupled receptor 40; Nodose ganglion; mercaptoacetate

Indexed keywords

CALCIUM; CAPSAICIN; CHOLECYSTOKININ; G PROTEIN COUPLED RECEPTOR 40; LINOLEIC ACID; OCTANOIC ACID; POTASSIUM ION; THIOGLYCOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; FATTY ACID OXIDATION; MALE; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; VAGUS NERVE;

CALCIUM IMAGING; FATTY ACIDS; G-PROTEIN COUPLED RECEPTOR 40; NODOSE GANGLION; Β-MERCAPTOACETATE;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CAPRYLATES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; EATING; FATTY ACIDS; LINOLEIC ACID; MALE; NODOSE GANGLION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SENSORY RECEPTOR CELLS; THIOGLYCOLATES; TIME FACTORS;

EID: 84903598127     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00536.2013     Document Type: Article

References (78)

1. + channels: a link between B-cell metabolism and insulin secretion. Biochem Soc Trans 18: 109-111, 1990.
2. Bauche F, Sabourault D, Giudicelli Y, Nordmann J, Nordmann R. 2-Mercaptoacetate administration depresses the β-oxidation pathway through an inhibition of long-chain acyl-CoA dehydrogenase activity. Biochem J 196: 803-809, 1981.
3. Bauche F, Sabourault D, Giudicelli Y, Nordmann J, Nordmann R. Inhibition in vitro of acyl-CoA dehydrogenases by 2-mercaptoacetate in rat liver mitochondria. Biochem J 215: 457-464, 1983.
4. Boneva NB, Kaplamadzhiev DB, Sahara S, Kikuchi H, Pyko IV, Kikuchi M, Tonchev AB, Yamashima T. Expression of fatty acidbinding proteins in adult hippocampal neurogenic niche of postischemic monkeys. Hippocampus 21: 162-171, 2011.
5. 3 adrenergic receptor agonist CL 316,243. Neurosci Lett 411: 104-107, 2007.
6. Briscoe CP, Peat AJ, McKeown SC, Corbett DF, Goetz AS, Littleton TR, McCoy DC, Kenakin TP, Andrews JL, Ammala C, Fornwald JA, Ignar DM, Jenkinson S. Pharmacological regulation of insulin secretion in MIN6 cells through the fatty acid receptor GPR40: identification of agonist and antagonist small molecules. Br J Pharmacol 148: 619-628, 2006.
7. Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, Eilert MM, Ellis C, Elshourbagy NA, Goetz AS, Minnick DT, Murdock PR, Sauls HR Jr, Shabon U, Spinage LD, Strum JC, Szekeres PG, Tan KB, Way JM, Ignar DM, Wilson S, Muir AI. The orphan G protein-coupled receptor GPR40 is activated by medium and long-chain fatty acids. J Biol Chem 278: 11303-11311, 2003.
8. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, Wise A, Dowell SJ. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278: 11312-11319, 2003.
9. Calingasan NY, Ritter S. Lateral parabrachial subnucleus lesions abolish feeding induced by mercaptoacetate but not by 2-deoxy-D-glucose. Am J Physiol Regul Integr Comp Physiol 265: R1168-R1178, 1993.
10. Cartoni C, Yasumatsu K, Ohkuri T, Shigemura N, Yoshida R, Godinot N, le Coutre J, Ninomiya Y, Damak S. Taste preference for fatty acids is mediated by GPR40 and GPR120. J Neurosci 30: 8376-8382, 2010.
11. Edfalk S, Steneberg P, Edlund H. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 57: 2280-2287, 2008.
12. Friedman MI, Tordoff MG, Ramirez I. Integrated metabolic control of food intake. Brain Res Bull 17: 855-859, 1986.
13. 2+ channel and link to insulin release. Am J Physiol Endocrinol Metab 289: E670-E677, 2005.
14. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, Tian H, Li Y. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology 149: 4519-4526, 2008.
15. Grabauskas G, Song I, Zhou S, Owyang C. Electrophysiological identification of glucose-sensing neurons in rat nodose ganglia. J Physiol 588: 617-632, 2010.
16. Gromada J. The free fatty acid receptor GPR40 generates excitement in pancreatic β-cells. Endocrinology 147: 672-673, 2006.
17. Gunthorpe MJ, Benham CD, Randall A, Davis JB. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci 23: 183-191, 2002.
18. Hara T, Hirasawa A, Ichimura A, Kimura I, Tsujimoto G. Free fatty acid receptors FFAR1 and GPR120 as novel therapeutic targets for metabolic disorders. J Pharm Sci 100: 3594-3601, 2011.
19. Hirasawa A, Hara T, Katsuma S, Adachi T, Tsujimoto G. Free fatty acid receptors and drug discovery. Biol Pharm Bull 31: 1847-1851, 2008.
20. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11: 90-94, 2005.
21. Holliday ND, Watson SJ, Brown AJ. Drug discovery opportunities and challenges at g protein coupled receptors for long chain free Fatty acids. Front Endocrinol (Lausanne) 2: 112, 2011.
22. Holzer HH, Turkelson CM, Solomon TE, Raybould HE. Intestinal lipid inhibits gastric emptying via CCK and a vagal capsaicin-sensitive afferent pathway in rats. Am J Physiol Gastrointest Liver Physiol 267: G625-G629, 1994.
23. Horn CC, Ji H, Friedman MI. Etomoxir, a fatty acid oxidation inhibitor, increases food intake and reduces hepatic energy status in rats. Physiol Behav 81: 157-162, 2004.
24. Hudson BD, Emanuel AJ, Wiater MF, Ritter S. The lipoprivic control of feeding is governed by fat metabolism, not by leptin or adipose depletion. Endocrinology 151: 2087-2096, 2010.
25. Ichimura A, Hirasawa A, Hara T, Tsujimoto G. Free fatty acid receptors act as nutrient sensors to regulate energy homeostasis. Prostaglandins Other Lipid Mediat 89: 82-88, 2009.
26. Ireland SJ, Tyers MB. Pharmacological characterization of 5-hydroxytryptamine-induced depolarization of the rat isolated vagus nerve. Br J Pharmacol 90: 229-238, 1987.
27. Itoh Y, Hinuma S. GPR40, a free fatty acid receptor on pancreatic beta cells, regulates insulin secretion. Hepatol Res 33: 171-173, 2005.
28. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422: 173-176, 2003.
29. Jambor de Sousa UL, Benthem L, Arsenijevic D, Scheurink AJ, Langhans W, Geary N, Leonhardt M. Hepatic-portal oleic acid inhibits feeding more potently than hepatic-portal caprylic acid in rats. Physiol Behav 89: 329-334, 2006.
30. Janssen S, Laermans J, Iwakura H, Tack J, Depoortere I. Sensing of fatty acids for octanoylation of ghrelin involves a gustatory G-protein. PLoS One 7: e40168, 2012.
31. + channels by intracellular ATP in human neocortical neurons. J Neurophysiol 77: 93-102, 1997.
32. Jordan SD, Konner AC, Bruning JC. Sensing the fuels: glucose and lipid signaling in the CNS controlling energy homeostasis. Cell Mol Life Sci 67: 3255-3273, 2010.
33. Kahler A, Zimmermann M, Langhans W. Suppression of hepatic fatty acid oxidation and food intake in men. Nutrition 15: 819-828, 1999.
34. Kilpatrick GJ, Jones BJ, Tyers MB. Binding of the 5-HT3 ligand, [3H]GR65630, to rat area postrema, vagus nerve and the brains of several species. Eur J Pharmacol 159: 157-164, 1989.
35. Lal S, Kirkup AJ, Brunsden AM, Thompson DG, Grundy D. Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol 281: G907-G915, 2001.
36. Lam TK, Schwartz GJ, Rossetti L. Hypothalamic sensing of fatty acids. Nat Neurosci 8: 579-584, 2005.
37. Langhans W. The enterocyte as an energy flow sensor in the control of eating. Forum Nutr 63: 75-84, 2010.
38. Langhans W. Fatty acid oxidation in the energostatic control of eating-a new idea. Appetite 51: 446-451, 2008.
39. Langhans W, Egli G, Scharrer E. Regulation of food intake by hepatic oxidative metabolism. Brain Res Bull 15: 425-428, 1985.
40. Langhans W, Leitner C, Arnold M. Dietary fat sensing via fatty acid oxidation in enterocytes: possible role in the control of eating. Am J Physiol Regul Integr Comp Physiol 300: R554-R565, 2011.
41. Langhans W, Scharrer E. Evidence for a vagally mediated satiety signal derived from hepatic fatty acid oxidation. J Auton Nerv Syst 18: 13-18, 1987.
42. Lee T, Schwandner R, Swaminath G, Weiszmann J, Cardozo M, Greenberg J, Jaeckel P, Ge H, Wang Y, Jiao X, Liu J, Kayser F, Tian H, Li Y. Identification and functional characterization of allosteric agonists for the G protein-coupled receptor FFA2. Mol Pharmacol 74: 1599-1609, 2008.
43. Leonhardt M, Langhans W. Fatty acid oxidation and control of food intake. Physiol Behav 83: 645-651, 2004.
44. Liou AP, Lu X, Sei Y, Zhao X, Pechhold S, Carrero RJ, Raybould HE, Wank S. The G-protein-coupled receptor GPR40 directly mediates longchain fatty acid-induced secretion of cholecystokinin. Gastroenterology 140: 903-912, 2011.
45. Lu X, Zhao X, Feng J, Liou AP, Anthony S, Pechhold S, Sun Y, Lu H, Wank S. Postprandial inhibition of gastric ghrelin secretion by long-chain fatty acid through GPR120 in isolated gastric ghrelin cells and mice. Am J Physiol Gastrointest Liver Physiol 303: G367-G376, 2012.
46. Lutz TA, Diener M, Scharrer E. Intraportal mercaptoacetate infusion increases afferent activity in the common hepatic vagus branch of the rat. Am J Physiol Regul Integr Comp Physiol 273: R442-R445, 1997.
47. Ma D, Lu L, Boneva NB, Warashina S, Kaplamadzhiev DB, Mori Y, Nakaya MA, Kikuchi M, Tonchev AB, Okano H, Yamashima T. Expression of free fatty acid receptor GPR40 in the neurogenic niche of adult monkey hippocampus. Hippocampus 18: 326-333, 2008.
48. Ma D, Tao B, Warashina S, Kotani S, Lu L, Kaplamadzhiev DB, Mori Y, Tonchev AB, Yamashima T. Expression of free fatty acid receptor GPR40 in the central nervous system of adult monkeys. Neurosci Res 58: 394-401, 2007.
49. Maggio CA, Koopmans HS. Food intake after intragastric meals of short-, medium-, or long-chain triglyceride. Physiol Behav 28: 921-926, 1982.
50. Mansouri A, Koss MD, Brandt K, Geary N, Langhans W, Leonhardt M. Dissociation of mercaptoacetate's effects on feeding and fat metabolism by dietary medium-and long-chain triacylglycerols in rats. Nutrition 24: 360-365, 2008.
51. Montell C, Birnbaumer L, Flockerzi V. The TRP channels, a remarkably functional family. Cell 108: 595-598, 2002.
52. Nilsson NE, Kotarsky K, Owman C, Olde B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by shortchain fatty acids. Biochem Biophys Res Commun 303: 1047-1052, 2003.
53. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, Li P, Lu WJ, Watkins SM, Olefsky JM. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142: 687-698, 2010.
54. Randich A, Spraggins DS, Cox JE, Meller ST, Kelm GR. Jejunal or portal vein infusions of lipids increase hepatic vagal afferent activity. Neuroreport 12: 3101-3105, 2001.
55. Randich A, Tyler WJ, Cox JE, Meller ST, Kelm GR, Bharaj SS. Responses of celiac and cervical vagal afferents to infusions of lipids in the jejunum or ileum of the rat. Am J Physiol Regul Integr Comp Physiol 278: R34-R43, 2000.
56. Rayasam GV, Tulasi VK, Davis JA, Bansal VS. Fatty acid receptors as new therapeutic targets for diabetes. Expert Opin Ther Targets 11: 661-671, 2007.
57. 2+-signaling in pancreatic β-cells. Mol Cell Endocrinol 212: 1-9, 2003.
58. Ritter RC, Ladenheim EE. Capsaicin pretreatment attenuates suppression of food intake by cholecystokinin. Am J Physiol Regul Integr Comp Physiol 248: R501-R504, 1985.
59. Ritter S, Calingasan NY. Neural substrates for metabolic controls of feeding. In: Appetite and Body Weight Regulation: Sugar, Fat, and Macronutrient Substitutes, edited by Fernstrom J and Miller G. D. Boca Raton, FL: CRC Press, 1994, p. 77-94.
60. Ritter S, Hutton B. Mercaptoacetate-induced feeding is impaired by central nucleus of the amygdala lesions. Physiol Behav 58: 1215-1220, 1995.
61. Ritter S, Li AJ, Wang Q, Simasko SM. Novel non-metabolic mechanism of action underlying 2-mercaptocacetate (MA)-induced feeding. In: 2013 Neuroscience Meeting Planner, San Diego, CA: Society for Neuroscience, 2013.
62. Ritter S, Taylor JS. Capsaicin abolishes lipoprivic but not glucoprivic feeding in rats. Am J Physiol Regul Integr Comp Physiol 256: R1232-R1239, 1989.
63. Ritter S, Taylor JS. Vagal sensory neurons are required for lipoprivic but not glucoprivic feeding in rats. Am J Physiol Regul Integr Comp Physiol 258: R1395-R1401, 1990.
64. Scharrer E, Langhans W. Control of food intake by fatty acid oxidation. Am J Physiol Regul Integr Comp Physiol 250: R1003-R1006, 1986.
65. Schioth HB. G protein-coupled receptors in regulation of body weight. CNS Neurol Disord Drug Targets 5: 241-249, 2006.
66. Simasko SM, Peters J, Weins J, Ritter RC. Co-activation of nodose ganglion neurons by cholecystokinin and serotonin. In: 2002 Neuroscience Meeting Planner, Orlando, FL: Society for Neuroscience, 2002.
67. Singer LK, Ritter S. Differential effects of infused nutrients on 2-deoxy-D-glucose-and 2-mercaptoacetate-induced feeding. Physiol Behav 56: 193-196, 1994.
68. Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol 121: 91-119, 2014.
69. Tutwiler GF, Brentzel HJ, Kiorpes TC. Inhibition of mitochondrial carnitine palmitoyl transferase A in vivo with methyl 2-tetradecylglycidate (methyl palmoxirate) and its relationship to ketonemia and glycemia. Proc Soc Exp Biol Med 178: 288-296, 1985.
70. van Dijk G, Scheurink A, Ritter S, Steffens A. Glucose homeostasis and sympathoadrenal activity in mercaptoacetate-treated rats. Physiol Behav 57: 759-764, 1995.
71. Wank SA. G protein-coupled receptors in gastrointestinal physiology. I. CCK receptors: an exemplary family. Am J Physiol Gastrointest Liver Physiol 274: G607-G613, 1998.
72. Wolf HP. Possible new therapeutic approach in diabetes mellitus by inhibition of carnitine palmitoyltransferase 1 (CPT1). Horm Metab Res Suppl 26: 62-67, 1992.
73. Xiong Y, Swaminath G, Cao Q, Yang L, Guo Q, Salomonis H, Lu J, Houze JB, Dransfield PJ, Wang Y, Liu JJ, Wong S, Schwandner R, Steger F, Baribault H, Liu L, Coberly S, Miao L, Zhang J, Lin DC, Schwarz M. Activation of FFA1 mediates GLP-1 secretion in mice. Evidence for allosterism at FFA1. Mol Cell Endocrinol 369: 119-129, 2013.
74. Yonezawa T, Kurata R, Yoshida K, Murayama MA, Cui X, Hasegawa A. Free fatty acids-sensing G protein-coupled receptors in drug targeting and therapeutics. Curr Med Chem 20: 3855-3871, 2013.
75. Yox DP, Ritter RC. Capsaicin attenuates suppression of sham feeding induced by intestinal nutrients. Am J Physiol Regul Integr Comp Physiol 255: R569-R574, 1988.
76. Yox DP, Stokesberry H, Ritter RC. Vagotomy attenuates suppression of sham feeding induced by intestinal nutrients. Am J Physiol Regul Integr Comp Physiol 260: R503-R508, 1991.
77. Zhao H, Simasko SM. Role of transient receptor potential channels in cholecystokinin-induced activation of cultured vagal afferent neurons. Endocrinology 151: 5237-5246, 2010.
78. + currents in pancreatic B-cells. Naunyn Schmiedebergs Arch Pharmacol 337: 225-230, 1988.