Free fatty acid receptor 1 (FFAR1/GPR40) signaling affects insulin secretion by enhancing mitochondrial respiration during palmitate exposure

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 12, 2015, Pages 3248-3257

  Kristinsson, Hjalti ^a   Bergsten, Peter ^a   Sargsyan, Ernest ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Fatty acid; FFAR1; GPR40; Insulin secretion; Mitochondrial respiration

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARBACHOL; ETOMOXIR; G PROTEIN COUPLED RECEPTOR 40; MITOCHONDRIAL DNA; MUSCARINIC M3 RECEPTOR; PALMITIC ACID; PROTEIN KINASE C; FFAR1 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; GPR40 PROTEIN, MOUSE; INSULIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FATTY ACID METABOLISM; GLUCOSE UTILIZATION; HUMAN; HUMAN CELL; INSULIN RELEASE; INTRACELLULAR SIGNALING; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; HEK293 CELL LINE; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; HEK293 CELLS; HUMANS; INSULIN; MICE; MITOCHONDRIA; OXYGEN CONSUMPTION; PALMITIC ACID; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84943577064     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.09.022     Document Type: Article

References (48)

1. Berne C. The metabolism of lipids in mouse pancreatic islets. The biosynthesis of triacylglycerols and phospholipids. Biochem. J. 1975, 152(3):667-673.
2. Prentki M., Vischer S., Glennon M.C., Regazzi R., Deeney J.T., Corkey B.E. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J. Biol. Chem. 1992, 267(9):5802-5810.
3. Sargsyan E., Bergsten P. Lipotoxicity is glucose-dependent in INS-1E cells but not in human islets and MIN6 cells. Lipids Health Dis. 2011, 10:115.
4. Prentki M., Madiraju S.R. Glycerolipid metabolism and signaling in health and disease. Endocr. Rev. 2008, 29(6):647-676.
5. Briscoe C.P., Tadayyon M., Andrews J.L., Benson W.G., Chambers J.K., Eilert M.M., et al. The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J. Biol. Chem. 2003, 278(13):11303-11311.
6. Itoh Y., Kawamata Y., Harada M., Kobayashi M., Fujii R., Fukusumi S., et al. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 2003, 422(6928):173-176.
7. + channel and link to insulin release. Am. J. Physiol. Endocrinol. Metab. 2005, 289(4):E670-E677.
8. Shapiro H., Shachar S., Sekler I., Hershfinkel M., Walker M.D. Role of GPR40 in fatty acid action on the beta cell line INS-1E. Biochem. Biophys. Res. Commun. 2005, 335(1):97-104.
9. Araki T., Hirayama M., Hiroi S., Kaku K. GPR40-induced insulin secretion by the novel agonist TAK-875: first clinical findings in patients with type 2 diabetes. Diabetes Obes. Metab. 2012, 14(3):271-278.
10. Burant C.F., Viswanathan P., Marcinak J., Cao C., Vakilynejad M., Xie B., et al. TAK-875 versus placebo or glimepiride in type 2 diabetes mellitus: a phase 2, randomised, double-blind, placebo-controlled trial. Lancet 2012, 379(9824):1403-1411.
11. Leifke E., Naik H., Wu J., Viswanathan P., Demanno D., Kipnes M., et al. A multiple-ascending-dose study to evaluate safety, pharmacokinetics, and pharmacodynamics of a novel GPR40 agonist, TAK-875, in subjects with type 2 diabetes. Clin. Pharmacol. Ther. 2012, 92(1):29-39.
12. Naik H., Vakilynejad M., Wu J., Viswanathan P., Dote N., Higuchi T., et al. Safety, tolerability, pharmacokinetics, and pharmacodynamic properties of the GPR40 agonist TAK-875: results from a double-blind, placebo-controlled single oral dose rising study in healthy volunteers. J. Clin. Pharmacol. 2012, 52(7):1007-1016.
13. Zhou Y.P., Grill V.E. Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J. Clin. Invest. 1994, 93(2):870-876.
14. Iizuka K., Nakajima H., Namba M., Miyagawa J., Miyazaki J., Hanafusa T., et al. Metabolic consequence of long-term exposure of pancreatic beta cells to free fatty acid with special reference to glucose insensitivity. Biochim. Biophys. Acta 2002, 1586(1):23-31.
15. Sargsyan E., Ortsater H., Thorn K., Bergsten P. Diazoxide-induced beta-cell rest reduces endoplasmic reticulum stress in lipotoxic beta-cells. J. Endocrinol. 2008, 199(1):41-50.
16. Manukyan L., Ubhayasekera S.J., Bergquist J., Sargsyan E., Bergsten P. Palmitate-induced impairments of beta-cell function are linked with generation of specific ceramide species via acylation of sphingosine. Endocrinology 2014.
17. Kristinsson H., Smith D.M., Bergsten P., Sargsyan E. FFAR1 is involved in both the acute and chronic effects of palmitate on insulin secretion. Endocrinology 2013, 154(11):4078-4088.
18. Natalicchio A., Labarbuta R., Tortosa F., Biondi G., Marrano N., Peschechera A., et al. Exendin-4 protects pancreatic beta cells from palmitate-induced apoptosis by interfering with GPR40 and the MKK4/7 stress kinase signalling pathway. Diabetologia 2013, 56(11):2456-2466.
19. Sun P., Wang T., Zhou Y., Liu H., Jiang H., Zhu W., et al. DC260126: a small-molecule antagonist of GPR40 that protects against pancreatic beta-cells dysfunction in db/db mice. PLoS One 2013, 8(6).
20. Wu J., Sun P., Zhang X., Liu H., Jiang H., Zhu W., et al. Inhibition of GPR40 protects MIN6 beta cells from palmitate-induced ER stress and apoptosis. J. Cell. Biochem. 2012, 113(4):1152-1158.
21. Affourtit C., Brand M.D. Stronger control of ATP/ADP by proton leak in pancreatic beta-cells than skeletal muscle mitochondria. Biochem. J. 2006, 393(Pt 1):151-159.
22. Kennedy E.D., Maechler P., Wollheim C.B. Effects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells. Diabetes 1998, 47(3):374-380.
23. Soejima A., Inoue K., Takai D., Kaneko M., Ishihara H., Oka Y., et al. Mitochondrial DNA is required for regulation of glucose-stimulated insulin secretion in a mouse pancreatic beta cell line, MIN6. J. Biol. Chem. 1996, 271(42):26194-26199.
24. Waring M.J., Baker D.J., Bennett S.N.L., Dossetter A.G., Garcia M.F.R., Georgsson J., et al. Discovery of a series of 2-(pyridinyl)pyrimidines as potent antagonists of GPR40. Med. Chem. Commun. 2015, 6(6):1024-1029.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
26. Malmgren S., Nicholls D.G., Taneera J., Bacos K., Koeck T., Tamaddon A., et al. Tight coupling between glucose and mitochondrial metabolism in clonal beta-cells is required for robust insulin secretion. J. Biol. Chem. 2009, 284(47):32395-32404.
27. Hu H., He L.Y., Gong Z., Li N., Lu Y.N., Zhai Q.W., et al. A novel class of antagonists for the FFAs receptor GPR40. Biochem. Biophys. Res. Commun. 2009, 390(3):557-563.
28. +-dependent interaction of S100A1 with F1-ATPase leads to an increased ATP content in cardiomyocytes. Mol. Cell. Biol. 2007, 27(12):4365-4373.
29. Denton R.M., Randle P.J., Martin B.R. Stimulation by calcium ions of pyruvate dehydrogenase phosphate phosphatase. Biochem. J. 1972, 128(1):161-163.
30. +-linked isocitrate dehydrogenase from the mitochondria of rat heart and other tissues. Biochem. J. 1978, 176(3):899-906.
31. + transfer to mitochondria. Cell 2010, 142(2):270-283.
32. Mahato B., Home P., Rajendran G., Paul A., Saha B., Ganguly A., et al. Regulation of mitochondrial function and cellular energy metabolism by protein kinase C-lambda/iota: a novel mode of balancing pluripotency. Stem Cells 2014, 32(11):2880-2892.
33. Sugawara K., Fujikawa M., Yoshida M. Screening of protein kinase inhibitors and knockdown experiments identified four kinases that affect mitochondrial ATP synthesis activity. FEBS Lett. 2013, 587(23):3843-3847.
34. Steneberg P., Rubins N., Bartoov-Shifman R., Walker M.D., Edlund H. The FFA receptor GPR40 links hyperinsulinemia, hepatic steatosis, and impaired glucose homeostasis in mouse. Cell Metab. 2005, 1(4):245-258.
35. Alquier T., Peyot M.L., Latour M.G., Kebede M., Sorensen C.M., Gesta S., et al. Deletion of GPR40 impairs glucose-induced insulin secretion in vivo in mice without affecting intracellular fuel metabolism in islets. Diabetes 2009, 58(11):2607-2615.
36. El-Azzouny M., Evans C.R., Treutelaar M.K., Kennedy R.T., Burant C.F. Increased glucose metabolism and glycerolipid formation by fatty acids and GPR40 receptor signaling underlies the fatty acid potentiation of insulin secretion. J. Biol. Chem. 2014, 289(19):13575-13588.
37. Yashiro H., Tsujihata Y., Takeuchi K., Hazama M., Johnson P.R., Rorsman P. The effects of TAK-875, a selective G protein-coupled receptor 40/free fatty acid 1 agonist, on insulin and glucagon secretion in isolated rat and human islets. J. Pharmacol. Exp. Ther. 2012, 340(2):483-489.
38. Chan C.B., De Leo D., Joseph J.W., McQuaid T.S., Ha X.F., Xu F., et al. Increased uncoupling protein-2 levels in beta-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 2001, 50(6):1302-1310.
39. Fleury C., Neverova M., Collins S., Raimbault S., Champigny O., Levi-Meyrueis C., et al. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat. Genet. 1997, 15(3):269-272.
40. Gutknecht J. Proton conductance caused by long-chain fatty acids in phospholipid bilayer membranes. J. Membr. Biol. 1988, 106(1):83-93.
41. Molina A.J., Wikstrom J.D., Stiles L., Las G., Mohamed H., Elorza A., et al. Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 2009, 58(10):2303-2315.
42. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416(1):15-18.
43. Mattiasson G., Shamloo M., Gido G., Mathi K., Tomasevic G., Yi S., et al. Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat. Med. 2003, 9(8):1062-1068.
44. Teshima Y., Akao M., Jones S.P., Marban E. Uncoupling protein-2 overexpression inhibits mitochondrial death pathway in cardiomyocytes. Circ. Res. 2003, 93(3):192-200.
45. Graciano M.F., Valle M.M., Curi R., Carpinelli A.R. Evidence for the involvement of GPR40 and NADPH oxidase in palmitic acid-induced superoxide production and insulin secretion. Islets 2013, 5(4):139-148.
46. Meidute Abaraviciene S., Lundquist I., Galvanovskis J., Flodgren E., Olde B., Salehi A. Palmitate-induced beta-cell dysfunction is associated with excessive NO production and is reversed by thiazolidinedione-mediated inhibition of GPR40 transduction mechanisms. PLoS One 2008, 3(5).
47. Wagner R., Kaiser G., Gerst F., Christiansen E., Due-Hansen M.E., Grundmann M., et al. Reevaluation of fatty acid receptor 1 as a drug target for the stimulation of insulin secretion in humans. Diabetes 2013, 62(6):2106-2111.
48. Kowaltowski A.J., de Souza-Pinto N.C., Castilho R.F., Vercesi A.E. Mitochondria and reactive oxygen species. Free Radic. Biol. Med. 2009, 47(4):333-343.