GPR41 modulates insulin secretion and gene expression in pancreatic b-cells and modifies metabolic homeostasis in fed and fasting states

FASEB Journal

Volumn 30, Issue 11, 2016, Pages 3860-3869

  Veprik, Anna ^a   Laufer, Dana ^a   Weiss, Sara ^a   Rubins, Nir ^a   Walker, Michael D ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Diabetes; Fasting; FFAR3; Glucose; Islet; SCFA

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 41; GLUCOSE; INSULIN; MESSENGER RNA; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; GPCR41 PROTEIN, MOUSE; VOLATILE FATTY ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; DIET RESTRICTION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE; HYPOGLYCEMIA; IN VITRO STUDY; INSULIN RELEASE; INSULIN SENSITIVITY; LOSS OF FUNCTION MUTATION; METABOLIC REGULATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; TRANSGENIC MOUSE; ANIMAL; GENE EXPRESSION; GENETICS; HOMEOSTASIS; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; FASTING; FATTY ACIDS, VOLATILE; GENE EXPRESSION; GLUCOSE; HOMEOSTASIS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MICE, TRANSGENIC; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84996553637     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201500030R     Document Type: Article

References (31)

1. Ichimura, A., Hasegawa, S., Kasubuchi, M., andKimura, I. (2014)Free fatty acid receptors as therapeutic targets for the treatment of diabetes. Front. Pharmacol. 5, 236
2. Bartoov-Shifman, R., Ridner, G., Bahar, K., Rubins, N., and Walker, M. D. (2007) Regulation of the gene encoding GPR40, a fatty acid receptor expressed selectively in pancreatic beta cells. J. Biol. Chem. 282, 23561-23571
3. Bahar Halpern, K., Veprik, A., Rubins, N., Naaman, O., and Walker, M. D. (2012) GPR41 gene expression is mediated by internal ribosome entry site (IRES)-dependent translation of bicistronic mRNA encoding GPR40 and GPR41 proteins. J. Biol. Chem. 287, 20154-20163
4. Brown, A. J., Goldsworthy, S.M., Barnes, A.A., Eilert, M.M., Tcheang, L., Daniels, D., Muir, A. I., Wigglesworth, M. J., Kinghorn, I., Fraser, N. J., Pike, N. B., Strum, J. C., Steplewski, K. M., Murdock, P. R., Holder, J. C., Marshall, F. H., Szekeres, P. G., Wilson, S., Ignar, D. M., Foord, S.M., Wise, A., andDowell, S. J. (2003)The orphanGproteincoupledreceptorsGPR41 andGPR43 are activatedbypropionate and other short chain carboxylic acids. J. Biol. Chem. 278, 11312-11319
5. Cummings, J. H., Pomare, E. W., Branch, W. J., Naylor, C. P., and Macfarlane, G. T. (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221-1227
6. Layden, B.T., Yalamanchi, S.K., Wolever, T.M., Dunaif, A., andLowe, W. L., Jr. (2012) Negative association of acetate with visceral adipose tissue and insulin levels. Diabetes Metab. Syndr. Obes. 5, 49-55
7. Wolever, T. M., Josse, R. G., Leiter, L. A., and Chiasson, J. L. (1997) Time of day andglucose tolerance status affect serumshort-chainfatty acid concentrations in humans. Metabolism 46, 805-811
8. Kimura, I., Inoue, D., Maeda, T., Hara, T., Ichimura, A., Miyauchi, S., Kobayashi, M., Hirasawa, A., and Tsujimoto, G. (2011) Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41).Proc.Natl.Acad. Sci. USA 108, 8030-8035
9. Won, Y.-J., Lu, V. B., Puhl III, H. L., and Ikeda, S. R. (2013) b-Hydroxybutyrate modulates N-Type calcium channels in rat sympathetic neurons by acting as an agonist for the G-proteincoupled receptor FFA3. J. Neurosci. 33, 19314-19325
10. Newman, J. C., and Verdin, E. (2014) Ketone bodies as signaling metabolites. Trends Endocrinol. Metab. 25, 42-52
11. Tang, C., Ahmed, K., Gille, A., Lu, S., Gröne, H.-J., Tunaru, S., and Offermanns, S. (2015) Loss of FFA2 and FFA3 increases insulin secretion and improves glucose tolerance in type 2 diabetes. Nat.Med. 21, 173-177
12. Ximenes, H.M.A., Hirata, A.E., Rocha, M. S., Curi, R., andCarpinelli, A. R. (2007) Propionate inhibits glucose-induced insulin secretion in isolated rat pancreatic islets. Cell Biochem. Funct. 25, 173-178
13. Bellahcene, M., O'Dowd, J. F., Wargent, E. T., Zaibi, M. S., Hislop, D. C., Ngala, R. A., Smith, D.M., Cawthorne, M. A., Stocker, C. J., and Arch, J. R. S. (2013) Male mice that lack the G-protein-coupled receptor GPR41 have low energy expenditure and increased body fat content. Br. J. Nutr. 109, 1755-1764
14. Lin, H. V., Frassetto, A., Kowalik, E. J., Jr., Nawrocki, A. R., Lu, M. M., Kosinski, J.R., Hubert, J. A., Szeto, D., Yao, X., Forrest, G., andMarsh, D. J. (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 7, e35240
15. De Vadder, F., Kovatcheva-Datchary, P., Goncalves, D., Vinera, J., Zitoun, C., Duchampt, A., Bäckhed, F., and Mithieux, G. (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156, 84-96
16. Li, D. S., Yuan, Y. H., Tu, H. J., Liang, Q. L., and Dai, L. J. (2009) A protocol for islet isolationfrommousepancreas. Nat. Protoc.4, 1649-1652
17. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y., and Yamamura, K. (1990) Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132
18. Huang, W., Sherman, B. T., and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists usingDAVIDbioinformatics resources. Nat. Protoc. 4, 44-57
19. Huang, W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
20. Brouwers, B., de Faudeur, G., Osipovich, A.B., Goyvaerts, L., Lemaire, K., Boesmans, L., Cauwelier, E. J.G., Granvik, M., Pruniau, V. P. E. G., VanLommel, L., VanSchoors, J., Stancill, J. S., Smolders, I., Goffin, V., Binart, N., in'tVeld, P., Declercq, J., Magnuson, M.A., Creemers, J.W., Schuit, F., and Schraenen, A. (2014) Impaired islet function in commonly used transgenic mouse lines due to human growth hormone minigene expression. Cell Metab. 20, 979-990
21. Samuel, B. S., Shaito, A., Motoike, T., Rey, F. E., Backhed, F., Manchester, J. K., Hammer, R. E., Williams, S. C., Crowley, J., Yanagisawa, M., and Gordon, J. I. (2008) Effects of the gutmicrobiota on host adiposity aremodulated by the short-chain fatty-Acid binding G protein-coupled receptor, Gpr41. Proc. Natl. Acad. Sci. USA 105, 16767-16772
22. Teutsch, C.-A., Panse, M., Grundmann, M., Kaiser, G., Kostenis, E., Häring, H.-U., and Ullrich, S. (2014) Detection of free fatty acid receptor 1 expression: The critical role of negative and positive controls. Diabetologia 57, 776-780
23. Hudson, B. D., Tikhonova, I. G., Pandey, S. K., Ulven, T., and Milligan, G. (2012) Extracellular ionic locks determine variation in constitutive activity and ligand potency between species orthologs of the free fatty acid receptors FFA2 and FFA3. J. Biol. Chem. 287, 41195-41209
24. Kassem, S., Bhandari, S., Rodŕiguez-Bada, P., Motaghedi, R., Heyman, M., Garćia-Gimeno, M. A., Cobo-Vuilleumier, N., Sanz, P., Maclaren, N. K., Rahier, J., Glaser, B., and Cuesta-Muñoz, A. L. (2010) Large islets, beta-cell proliferation, and a glucokinase mutation. N. Engl. J. Med. 362, 1348-1350
25. Porat, S., Weinberg-Corem, N., Tornovsky-Babaey, S., Schyr-Ben-Haroush, R., Hija, A., Stolovich-Rain, M., Dadon, D., Granot, Z., Ben-Hur, V., White, P., Girard, C. A., Karni, R., Kaestner, K. H., Ashcroft, F. M., Magnuson, M.A., Saada, A., Grimsby, J., Glaser, B., andDor, Y. (2011) Control of pancreatic b cell regeneration by glucosemetabolism. Cell Metab. 13, 440-449
26. Böni-Schnetzler, M., Boller, S., Debray, S., Bouzakri, K., Meier, D. T., Prazak, R., Kerr-Conte, J., Pattou, F., Ehses, J. A., Schuit, F. C., and Donath, M. Y. (2009) Free fatty acids induce a proinflammatory response in islets via the abundantly expressed interleukin-1 receptor I. Endocrinology 150, 5218-5229
27. Ehses, J. A., Perren, A., Eppler, E., Ribaux, P., Pospisilik, J. A., Maor-Cahn, R., Gueripel, X., Ellingsgaard, H., Schneider, M. K. J., Biollaz, G., Fontana, A., Reinecke, M., Homo-Delarche, F., and Donath, M. Y. (2007) Increased number of islet-Associated macrophages in type 2 diabetes. Diabetes 56, 2356-2370
28. Priyadarshini, M., and Layden, B. T. (2015) FFAR3modulates insulin secretionandglobal geneexpressioninmouse islets. Islets 7, e1045182
29. Shah, J.H., Wongsurawat, N., and Aran, P. P. (1977) Effect of ethanol on stimulus-induced insulin secretion and glucose tolerance. A study of mechanisms. Diabetes 26, 271-277
30. Patel, D. G., and Singh, S. P. (1979) Effect of ethanol and its metabolites on glucosemediated insulin release fromisolated islets of rats. Metabolism 28, 85-89
31. Ahŕen, B. (2009) IsletGprotein-coupledreceptors aspotential targets for treatment of type 2 diabetes. Nat. Rev. Drug Discov. 8, 369-385