α/β-Hydrolase Domain-6-accessible monoacylglycerol controls glucose-stimulated insulin secretion

Cell Metabolism

Volumn 19, Issue 6, 2014, Pages 993-1007

  Zhao, Shangang ^a   Mugabo, Yves ^a   Iglesias, Jose ^a   Xie, Li ^b   Delghingaro Augusto, Viviane ^a   Lussier, Roxane ^a   Peyot, Marie Line ^a   Joly, Erik ^a   Taïb, Bouchra ^c   Davis, Matthew A ^d   Brown, J Mark ^d   Abousalham, Abdelkarim ^e   Gaisano, Herbert ^b   Madiraju, S R Murthy ^a   Prentki, Marc ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

^e UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CRE RECOMBINASE; FATTY ACID; GLUCOSE; INSULIN; MONOACYLGLYCEROL; MONOACYLGLYCEROL LIPASE ALPHA BETA HYDROLASE DOMAIN 6; SMALL INTERFERING RNA; TETRAHYDROLIPSTATIN; TRYPTOPHAN; UNCLASSIFIED DRUG; ABHD6 PROTEIN, MOUSE; ANTIOBESITY AGENT; BIPHENYL DERIVATIVE; CARBAMIC ACID DERIVATIVE; ENZYME INHIBITOR; LACTONE; N-METHYL-N-((3-(4-PYRIDINYL)PHENYL)METHYL)-4'-(AMINOCARBONYL)(1,1'-BIPHENYL)-4-YL ESTER, CARBAMIC ACID; NERVE PROTEIN; PROTEIN BINDING; TRIACYLGLYCEROL LIPASE; UNC13A PROTEIN, MOUSE; ALPHA BETA HYDROLASE DOMAIN 6; MUNC 13 PROTIEN; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COUPLING FACTOR; EX VIVO STUDY; EXOCYTOSIS; FOOD INTAKE; GENE DELETION; GENE SILENCING; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HYDROLYSIS; IN VIVO STUDY; INSULIN RELEASE; INSULINEMIA; LIPOLYSIS; MALE; MOUSE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; WEIGHT GAIN; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; HUMAN; KNOCKOUT MOUSE; LIPID METABOLISM; METABOLISM; RAT; RNA INTERFERENCE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; WISTAR RAT; B LYMPHOCYTE; CELL STIMULATION; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCONEOGENESIS; GRANULE CELL; MEMBRANE FUSION;

ANIMALS; ANTI-OBESITY AGENTS; BIPHENYL COMPOUNDS; CARBAMATES; CELLS, CULTURED; ENZYME INHIBITORS; GLUCOSE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; LACTONES; LIPASE; LIPID METABOLISM; LIPOLYSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOACYLGLYCEROL LIPASES; MONOGLYCERIDES; NERVE TISSUE PROTEINS; PROTEIN BINDING; RATS; RATS, WISTAR; RECEPTORS, CANNABINOID; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84902270757     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.04.003     Document Type: Article

References (54)

1. M. Alhouayek, J. Masquelier, P.D. Cani, D.M. Lambert, and G.G. Muccioli Implication of the anti-inflammatory bioactive lipid prostaglandin D2-glycerol ester in the control of macrophage activation and inflammation by ABHD6 Proc. Natl. Acad. Sci. USA 110 2013 17558 17563
2. F.M. Ashcroft, and P. Rorsman Diabetes mellitus and the β cell: the last ten years Cell 148 2012 1160 1171
3. I. Augustin, C. Rosenmund, T.C. Südhof, and N. Brose Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles Nature 400 1999 457 461
4. D.A. Bachovchin, T. Ji, W. Li, G.M. Simon, J.L. Blankman, A. Adibekian, H. Hoover, S. Niessen, and B.F. Cravatt Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening Proc. Natl. Acad. Sci. USA 107 2010 20941 20946
5. S. Ben-Shabat, E. Fride, T. Sheskin, T. Tamiri, M.H. Rhee, Z. Vogel, T. Bisogno, L. De Petrocellis, V. Di Marzo, and R. Mechoulam An entourage effect: inactive endogenous fatty acid glycerol esters enhance 2-arachidonoyl-glycerol cannabinoid activity Eur. J. Pharmacol. 353 1998 23 31
6. J.L. Blankman, G.M. Simon, and B.F. Cravatt A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol Chem. Biol. 14 2007 1347 1356
7. P.T. Bozza, I. Bakker-Abreu, R.A. Navarro-Xavier, and C. Bandeira-Melo Lipid body function in eicosanoid synthesis: an update Prostaglandins Leukot. Essent. Fatty Acids 85 2011 205 213
8. T.O. Eichmann, M. Kumari, J.T. Haas, R.V. Farese Jr., R. Zimmermann, A. Lass, and R. Zechner Studies on the substrate and stereo/regioselectivity of adipose triglyceride lipase, hormone-sensitive lipase, and diacylglycerol-O- acyltransferases J. Biol. Chem. 287 2012 41446 41457
9. L. Eliasson, F. Abdulkader, M. Braun, J. Galvanovskis, M.B. Hoppa, and P. Rorsman Novel aspects of the molecular mechanisms controlling insulin secretion J. Physiol. 586 2008 3313 3324
10. M. Fex, G. Haemmerle, N. Wierup, M. Dekker-Nitert, M. Rehn, M. Ristow, R. Zechner, F. Sundler, C. Holm, L. Eliasson, and H. Mulder A beta cell-specific knockout of hormone-sensitive lipase in mice results in hyperglycaemia and disruption of exocytosis Diabetologia 52 2009 271 280
11. K.D. Gillis, R. Mossner, and E. Neher Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules Neuron 16 1996 1209 1220
12. C.D. Green, D.B. Jump, and L.K. Olson Elevated insulin secretion from liver X receptor-activated pancreatic beta-cells involves increased de novo lipid synthesis and triacylglyceride turnover Endocrinology 150 2009 2637 2645
13. A. Guenifi, E. Simonsson, S. Karlsson, B. Ahrén, and S.M. Abdel-Halim Carbachol restores insulin release in diabetic GK rat islets by mechanisms largely involving hydrolysis of diacylglycerol and direct interaction with the exocytotic machinery Pancreas 22 2001 164 171
14. G. Haemmerle, R. Zimmermann, M. Hayn, C. Theussl, G. Waeg, E. Wagner, W. Sattler, T.M. Magin, E.F. Wagner, and R. Zechner Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis J. Biol. Chem. 277 2002 4806 4815
15. K. Hayashi, R. Kojima, and M. Ito Strain differences in the diabetogenic activity of streptozotocin in mice Biol. Pharm. Bull. 29 2006 1110 1119
16. J.C. Henquin The dual control of insulin secretion by glucose involves triggering and amplifying pathways in β-cells Diabetes Res. Clin. Pract. 93 Suppl 1 2011 S27 S31
17. H.E. Hohmeier, H. Mulder, G. Chen, R. Henkel-Rieger, M. Prentki, and C.B. Newgard Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion Diabetes 49 2000 424 430
18. Y. Iwasaki, O. Saito, M. Tanabe, K. Inayoshi, K. Kobata, S. Uno, A. Morita, and T. Watanabe Monoacylglycerols activate capsaicin receptor, TRPV1 Lipids 43 2008 471 483
19. S. Jitrapakdee, A. Wutthisathapornchai, J.C. Wallace, and M.J. MacDonald Regulation of insulin secretion: role of mitochondrial signalling Diabetologia 53 2010 1019 1032
20. W. Kim, M.E. Doyle, Z. Liu, Q. Lao, Y.K. Shin, O.D. Carlson, H.S. Kim, S. Thomas, J.K. Napora, and E.K. Lee et al. Cannabinoids inhibit insulin receptor signaling in pancreatic β-cells Diabetes 60 2011 1198 1209
21. E.P. Kwan, and H.Y. Gaisano Rescuing the subprime meltdown in insulin exocytosis in diabetes Ann. N Y Acad. Sci. 1152 2009 154 164
22. E.P. Kwan, L. Xie, L. Sheu, C.J. Nolan, M. Prentki, A. Betz, N. Brose, and H.Y. Gaisano Munc13-1 deficiency reduces insulin secretion and causes abnormal glucose tolerance Diabetes 55 2006 1421 1429
23. R. Lan, Q. Liu, P. Fan, S. Lin, S.R. Fernando, D. McCallion, R. Pertwee, and A. Makriyannis Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists J. Med. Chem. 42 1999 769 776
24. A. Lass, R. Zimmermann, M. Oberer, and R. Zechner Lipolysis - a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores Prog. Lipid Res. 50 2011 14 27
25. C. Li, A. Vilches-Flores, M. Zhao, S.A. Amiel, P.M. Jones, and S.J. Persaud Expression and function of monoacylglycerol lipase in mouse β-cells and human islets of Langerhans Cell. Physiol. Biochem. 30 2012 347 358
26. J.Z. Long, D.K. Nomura, and B.F. Cravatt Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism Chem. Biol. 16 2009 744 753
27. C. Ma, L. Su, A.B. Seven, Y. Xu, and J. Rizo Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release Science 339 2013 421 425
28. P.E. MacDonald Signal integration at the level of ion channel and exocytotic function in pancreatic β-cells Am. J. Physiol. Endocrinol. Metab. 301 2011 E1065 E1069
29. P. Maechler, and C.B. Wollheim Role of mitochondria in metabolism-secretion coupling of insulin release in the pancreatic beta-cell Biofactors 8 1998 255 262
30. W.R. Marrs, J.L. Blankman, E.A. Horne, A. Thomazeau, Y.H. Lin, J. Coy, A.L. Bodor, G.G. Muccioli, S.S. Hu, and G. Woodruff et al. The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors Nat. Neurosci. 13 2010 951 957
31. I. Matias, M.P. Gonthier, P. Orlando, V. Martiadis, L. De Petrocellis, C. Cervino, S. Petrosino, L. Hoareau, F. Festy, and R. Pasquali et al. Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia J. Clin. Endocrinol. Metab. 91 2006 3171 3180
32. D. Navia-Paldanius, J.R. Savinainen, and J.T. Laitinen Biochemical and pharmacological characterization of human α/β-hydrolase domain containing 6 (ABHD6) and 12 (ABHD12) J. Lipid Res. 53 2012 2413 2424
33. C.J. Nolan, and M. Prentki The islet beta-cell: fuel responsive and vulnerable Trends Endocrinol. Metab. 19 2008 285 291
34. C.J. Nolan, J.L. Leahy, V. Delghingaro-Augusto, J. Moibi, K. Soni, M.L. Peyot, M. Fortier, C. Guay, J. Lamontagne, and A. Barbeau et al. Beta cell compensation for insulin resistance in Zucker fatty rats: increased lipolysis and fatty acid signalling Diabetologia 49 2006 2120 2130
35. C.J. Nolan, M.S. Madiraju, V. Delghingaro-Augusto, M.L. Peyot, and M. Prentki Fatty acid signaling in the beta-cell and insulin secretion Diabetes 55 Suppl 2 2006 S16 S23
36. M.L. Peyot, C.J. Nolan, K. Soni, E. Joly, R. Lussier, B.E. Corkey, S.P. Wang, G.A. Mitchell, and M. Prentki Hormone-sensitive lipase has a role in lipid signaling for insulin secretion but is nonessential for the incretin action of glucagon-like peptide 1 Diabetes 53 2004 1733 1742
37. M.L. Peyot, C. Guay, M.G. Latour, J. Lamontagne, R. Lussier, M. Pineda, N.B. Ruderman, G. Haemmerle, R. Zechner, and E. Joly et al. Adipose triglyceride lipase is implicated in fuel- and non-fuel-stimulated insulin secretion J. Biol. Chem. 284 2009 16848 16859
38. M. Prentki, and S.R. Madiraju Glycerolipid/free fatty acid cycle and islet β-cell function in health, obesity and diabetes Mol. Cell. Endocrinol. 353 2012 88 100
39. M. Prentki, and F.M. Matschinsky Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion Physiol. Rev. 67 1987 1185 1248
40. M. Prentki, F.M. Matschinsky, and S.R. Madiraju Metabolic signaling in fuel-induced insulin secretion Cell Metab. 18 2013 162 185
41. J.S. Rhee, A. Betz, S. Pyott, K. Reim, F. Varoqueaux, I. Augustin, D. Hesse, T.C. Südhof, M. Takahashi, C. Rosenmund, and N. Brose Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs Cell 108 2002 121 133
42. R. Roduit, C. Nolan, C. Alarcon, P. Moore, A. Barbeau, V. Delghingaro-Augusto, E. Przybykowski, J. Morin, F. Massé, and B. Massie et al. A role for the malonyl-CoA/long-chain acyl-CoA pathway of lipid signaling in the regulation of insulin secretion in response to both fuel and nonfuel stimuli Diabetes 53 2004 1007 1019
43. P. Rorsman, and E. Renström Insulin granule dynamics in pancreatic beta cells Diabetologia 46 2003 1029 1045
44. R.A. Ross, H.C. Brockie, L.A. Stevenson, V.L. Murphy, F. Templeton, A. Makriyannis, and R.G. Pertwee Agonist-inverse agonist characterization at CB1 and CB2 cannabinoid receptors of L759633, L759656, and AM630 Br. J. Pharmacol. 126 1999 665 672
45. D.L. Severson, and M. Hee-Cheong Monoacylglycerol lipase activity in cardiac myocytes Biochem. Cell Biol. 66 1988 1013 1018
46. N. Shen, O. Guryev, and J. Rizo Intramolecular occlusion of the diacylglycerol-binding site in the C1 domain of munc13-1 Biochemistry 44 2005 1089 1096
47. L. Sheu, E.A. Pasyk, J. Ji, X. Huang, X. Gao, F. Varoqueaux, N. Brose, and H.Y. Gaisano Regulation of insulin exocytosis by Munc13-1 J. Biol. Chem. 278 2003 27556 27563
48. D. Siow, and B. Wattenberg The compartmentalization and translocation of the sphingosine kinases: mechanisms and functions in cell signaling and sphingolipid metabolism Crit. Rev. Biochem. Mol. Biol. 46 2011 365 375
49. W.C. Skarnes, B. Rosen, A.P. West, M. Koutsourakis, W. Bushell, V. Iyer, A.O. Mujica, M. Thomas, J. Harrow, and T. Cox et al. A conditional knockout resource for the genome-wide study of mouse gene function Nature 474 2011 337 342
50. G. Thomas, J.L. Betters, C.C. Lord, A.L. Brown, S. Marshall, D. Ferguson, J. Sawyer, M.A. Davis, J.T. Melchior, and L.C. Blume et al. The serine hydrolase ABHD6 Is a critical regulator of the metabolic syndrome Cell Rep. 5 2013 508 520
51. S. Vandevoorde, K.O. Jonsson, G. Labar, E. Persson, D.M. Lambert, and C.J. Fowler Lack of selectivity of URB602 for 2-oleoylglycerol compared to anandamide hydrolysis in vitro Br. J. Pharmacol. 150 2007 186 191
52. B. Wicksteed, M. Brissova, W. Yan, D.M. Opland, J.L. Plank, R.B. Reinert, L.M. Dickson, N.A. Tamarina, L.H. Philipson, and A. Shostak et al. Conditional gene targeting in mouse pancreatic ß-Cells: analysis of ectopic Cre transgene expression in the brain Diabetes 59 2010 3090 3098
53. J. Wiskerke, C. Irimia, B.F. Cravatt, T.J. De Vries, A.N. Schoffelmeer, T. Pattij, and L.H. Parsons Characterization of the effects of reuptake and hydrolysis inhibition on interstitial endocannabinoid levels in the brain: an in vivo microdialysis study ACS Chem. Neurosci. 3 2012 407 417
54. P.M. Zygmunt, A. Ermund, P. Movahed, D.A. Andersson, C. Simonsen, B.A. Jönsson, A. Blomgren, B. Birnir, S. Bevan, and A. Eschalier et al. Monoacylglycerols activate TRPV1 - a link between phospholipase C and TRPV1 PLoS ONE 8 2013 e81618