The Serine Hydrolase ABHD6 Is a Critical Regulator of the Metabolic Syndrome

Cell Reports

Volumn 5, Issue 2, 2013, Pages 508-520

  Thomas, Gwynneth ^a   Betters, Jenna L ^a   Lord, Caleb C ^a   Brown, Amanda L ^a,b   Marshall, Stephanie ^a,b   Ferguson, Daniel ^a,b   Sawyer, Janet ^a   Davis, Matthew A ^a   Melchior, John T ^a   Blume, Lawrence C ^a   Howlett, Allyn C ^a   Ivanova, Pavlina T ^c   Milne, Stephen B ^c   Myers, David S ^c   Mrak, Irina ^d   Leber, Vera ^d   Heier, Christoph ^d   Taschler, Ulrike ^d   Blankman, Jacqueline L ^e   Cravatt, Benjamin F ^e   Lee, Richard G ^f   Crooke, Rosanne M ^f   Graham, Mark J ^f   Zimmermann, Robert ^d   Brown, H Alex ^c   Brown, J Mark ^a,b   more..

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF GRAZ   (Austria)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f ISIS PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA HYDROLASE DOMAIN 6; ANTISENSE OLIGONUCLEOTIDE; CANNABINOID 1 RECEPTOR; CHOLESTEROL; ENDOCANNABINOID; FATTY ACID; GLUCOSE; HYDROLASE; MESSENGER RNA; UNCLASSIFIED DRUG; ABHD6 PROTEIN, MOUSE; ACYLGLYCEROL LIPASE; CNR1 PROTEIN, RAT;

ABHD6 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FATTY ACID SYNTHESIS; FATTY LIVER; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; HYPERCHOLESTEROLEMIA; HYPERGLYCEMIA; HYPERINSULINEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; LIPID DIET; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; ENZYMOLOGY; GENETICS; HUMAN; LIVER; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; SEQUENCE ALIGNMENT;

MUS;

AMINO ACID SEQUENCE; ANIMALS; DIET, HIGH-FAT; ENDOCANNABINOIDS; FATTY ACIDS; HUMANS; LIVER; MALE; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MONOACYLGLYCEROL LIPASES; OBESITY; OLIGONUCLEOTIDES, ANTISENSE; RECEPTOR, CANNABINOID, CB1; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 84887014824     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.08.047     Document Type: Article

References (38)

1. Bachovchin D.A., Ji T., Li W., Simon G.M., Blankman J.L., Adibekian A., Hoover H., Niessen S., Cravatt B.F. Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening. Proc. Natl. Acad. Sci. USA 2010, 107:20941-20946.
2. Blankman J.L., Simon G.M., Cravatt B.F. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol. 2007, 14:1347-1356.
3. Blankman J.L., Long J.Z., Trauger S.A., Siuzdak G., Cravatt B.F. ABHD12 controls brain lysophosphatidylserine pathways that are deregulated in a murine model of the neurodegenerative disease PHARC. Proc. Natl. Acad. Sci. USA 2013, 110:1500-1505.
4. Brown J.M., Boysen M.S., Chung S., Fabiyi O., Morrison R.F., Mandrup S., McIntosh M.K. Conjugated linoleic acid induces human adipocyte delipidation: autocrine/paracrine regulation of MEK/ERK signaling by adipocytokines. J.Biol. Chem. 2004, 279:26735-26747.
5. Brown J.M., Chung S., Sawyer J.K., Degirolamo C., Alger H.M., Nguyen T., Zhu X., Duong M.N., Wibley A.L., Shah R., et al. Inhibition of stearoyl-coenzyme A desaturase 1 dissociates insulin resistance and obesity from atherosclerosis. Circulation 2008, 118:1467-1475.
6. Brown J.M., Bell T.A., Alger H.M., Sawyer J.K., Smith T.L., Kelley K., Shah R., Wilson M.D., Davis M.A., Lee R.G., et al. Targeted depletion of hepatic ACAT2-driven cholesterol esterification reveals a non-biliary route for fecal neutral sterol loss. J.Biol. Chem. 2008, 283:10522-10534.
7. Brown J.M., Betters J.L., Lord C., Ma Y., Han X., Yang K., Alger H.M., Melchior J., Sawyer J.K., Shah R., et al. CGI-58 knockdown in mice causes hepatic steatosis but prevents diet-induced obesity and glucose intolerance. J.Lipid Res. 2010, 51:3306-3315.
8. Callender H.L., Forrester J.S., Ivanova P., Preininger A., Milne S., Brown H.A. Quantification of diacylglycerol species from cellular extracts by electrospray ionization mass spectrometry using a linear regression algorithm. Anal. Chem. 2007, 79:263-272.
9. Crooke S.T. Advances in understanding the pharmacological properties of antisense oligonucleotides. Adv. Pharmacol. 1997, 40:1-49.
10. Fiskerstrand T., H'mida-Ben Brahim D., Johansson S., M'zahem A., Haukanes B.I., Drouot N., Zimmermann J., Cole A.J., Vedeler C., Bredrup C., et al. Mutations in ABHD12 cause the neurodegenerative disease PHARC: An inborn error of endocannabinoid metabolism. Am. J. Hum. Genet. 2010, 87:410-417.
11. Hotelier T., Renault L., Cousin X., Negre V., Marchot P., Chatonnet A. ESTHER, the database of the alpha/beta-hydrolase fold superfamily of proteins. Nucleic Acids Res. 2004, 32(Database issue):D145-D147.
12. Hullin-Matsuda F., Kawasaki K., Delton-Vandenbroucke I., Xu Y., Nishijima M., Lagarde M., Schlame M., Kobayashi T. De novo biosynthesis of the late endosome lipid, bis(monoacylglycero)phosphate. J.Lipid Res. 2007, 48:1997-2008.
13. Ivanova P.T., Milne S.B., Byrne M.O., Xiang Y., Brown H.A. Glycerophospholipid identification and quantitation by electrospray ionization mass spectrometry. Methods Enzymol. 2007, 432:21-57.
14. Jandacek R.J., Heubi J.E., Tso P. A novel, noninvasive method for the measurement of intestinal fat absorption. Gastroenterology 2004, 127:139-144.
15. Jo S.H., Kim S.D., Kim J.M., Lee H.Y., Lee S.Y., Shim J.W., Yun J., Im D.S., Bae Y.S. Lysophosphatidylglycerol stimulates chemotactic migration in human natural killer cells. Biochem. Biophys. Res. Commun. 2008, 372:147-151.
16. Lefèvre C., Jobard F., Caux F., Bouadjar B., Karaduman A., Heilig R., Lakhdar H., Wollenberg A., Verret J.L., Weissenbach J., et al. Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome. Am. J. Hum. Genet. 2001, 69:1002-1012.
17. Lass A., Zimmermann R., Haemmerle G., Riederer M., Schoiswohl G., Schweiger M., Kienesberger P., Strauss J.G., Gorkiewicz G., Zechner R. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome. Cell Metab. 2006, 3:309-319.
18. Li X., Catalina F., Grundy S.M., Patel S. Method to measure apolipoprotein B-48 and B-100 secretion rates in an individual mouse: evidence for a very rapid turnover of VLDL and preferential removal of B-48- relative to B-100-containing lipoproteins. J.Lipid Res. 1996, 37:210-220.
19. Long J.Z., Nomura D.K., Cravatt B.F. Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism. Chem. Biol. 2009, 16:744-753.
20. Long J.Z., Cisar J.S., Milliken D., Niessen S., Wang C., Trauger S.A., Siuzdak G., Cravatt B.F. Metabolomics annotates ABHD3 as a physiologic regulator of medium-chain phospholipids. Nat. Chem. Biol. 2011, 7:763-765.
21. Lord C.C., Betters J.L., Ivanova P.T., Milne S.B., Myers D.S., Madenspacher J., Thomas G., Chung S., Liu M., Davis M.A., et al. CGI-58/ABHD5-derived signaling lipids regulate systemic inflammation and insulin action. Diabetes 2012, 61:355-363.
22. Makide K., Kitamura H., Sato Y., Okutani M., Aoki J. Emerging lysophospholipid mediators, lysophosphatidylserine, lysophosphatidylthreonine, lysophosphatidylethanolamine and lysophosphatidylglycerol. Prostaglandins Other Lipid Mediat. 2009, 89:135-139.
23. Marrs W.R., Blankman J.L., Horne E.A., Thomazeau A., Lin Y.H., Coy J., Bodor A.L., Muccioli G.G., Hu S.S., Woodruff G., et al. The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat. Neurosci. 2010, 13:951-957.
24. Marrs W.R., Horne E.A., Ortega-Gutierrez S., Cisneros J.A., Xu C., Lin Y.H., Muccioli G.G., Lopez-Rodriguez M.L., Stella N. Dual inhibition of alpha/beta-hydrolase domain 6 and fatty acid amide hydrolase increases endocannabinoid levels in neurons. J.Biol. Chem. 2011, 286:28723-28728.
25. Montero-Moran G., Caviglia J.M., McMahon D., Rothenberg A., Subramanian V., Xu Z., Lara-Gonzalez S., Storch J., Carman G.M., Brasaemle D.L. CGI-58/ABHD5 is a coenzyme A-dependent lysophosphatidic acid acyltransferase. J.Lipid Res. 2010, 51:709-719.
26. Myers D.S., Ivanova P.T., Milne S.B., Brown H.A. Quantitative analysis of glycerophospholipids by LC-MS: acquisition, data handling, and interpretation. Biochim. Biophys. Acta 2011, 1811:748-757.
27. Nardini M., Dijkstra B.W. Alpha/beta hydrolase fold enzymes: the family keeps growing. Curr. Opin. Struct. Biol. 1999, 9:732-737.
28. Navia-Paldanius D., Savinainen J.R., Laitinen J.T. Biochemical and pharmacological characterization of human α/β-hydrolase domain containing 6 (ABHD6) and 12 (ABHD12). J.Lipid Res. 2012, 53:2413-2424.
29. Osei-Hyiaman D., DePetrillo M., Pacher P., Liu J., Radaeva S., Bátkai S., Harvey-White J., Mackie K., Offertáler L., Wang L., Kunos G. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J.Clin. Invest. 2005, 115:1298-1305.
30. Osei-Hyiaman D., Liu J., Zhou L., Godlewski G., Harvey-White J., Jeong W.I., Bátkai S., Marsicano G., Lutz B., Buettner C., Kunos G. Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice. J.Clin. Invest. 2008, 118:3160-3169.
31. Schlosburg J.E., Blankman J.L., Long J.Z., Nomura D.K., Pan B., Kinsey S.G., Nguyen P.T., Ramesh D., Booker L., Burston J.J., et al. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci. 2010, 13:1113-1119.
32. Schweiger M., Lass A., Zimmermann R., Eichmann T.O., Zechner R. Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E289-E296.
33. Shimano H., Horton J.D., Hammer R.E., Shimomura I., Brown M.S., Goldstein J.L. Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J.Clin. Invest. 1996, 98:1575-1584.
34. Simon G.M., Cravatt B.F. Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway. J.Biol. Chem. 2006, 281:26465-26472.
35. Skoura A., Hla T. Lysophospholipid receptors in vertebrate development, physiology, and pathology. J.Lipid Res. 2009, 50(Suppl):S293-S298.
36. Taschler U., Radner F.P., Heier C., Schreiber R., Schweiger M., Schoiswohl G., Preiss-Landl K., Jaeger D., Reiter B., Koefeler H.C., et al. Monoglyceride lipase deficiency in mice impairs lipolysis and attenuates diet-induced insulin resistance. J.Biol. Chem. 2011, 286:17467-17477.
37. Traurig M.T., Orczewska J.I., Ortiz D.J., Bian L., Marinelarena A.M., Kobes S., Malhotra A., Hanson R.L., Mason C.C., Knowler W.C., et al. Evidence for a role of LPGAT1 in influencing BMI and percent body fat in Native Americans. Obesity (Silver Spring) 2013, 21:193-202.
38. Wymann M.P., Schneiter R. Lipid signalling in disease. Nat. Rev. Mol. Cell Biol. 2008, 9:162-176.