Identification of N-acylethanolamines in Dictyostelium discoideum and confirmation of their hydrolysis by fatty acid amide hydrolase

Journal of Lipid Research

Volumn 54, Issue 2, 2013, Pages 457-466

  Hayes, Alexander C ^a   Stupak, Jacek ^a   Li, Jianjun ^a   Cox, Andrew D ^a  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Anandamide; Endocannabinoid; N acylethanolamine

Indexed keywords

ETHANOLAMINE; FATTY ACID AMIDASE; FATTY ACID AMIDASE INHIBITOR; N ACYLETHANOLAMINE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; LIPID ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMIDOHYDROLASES; ANIMALS; COMPUTATIONAL BIOLOGY; DICTYOSTELIUM; ENZYME INHIBITORS; ETHANOLAMINES; HUMANS; HYDROLYSIS; KINETICS; MICE; PHYLOGENY;

EID: 84872459161     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M032219     Document Type: Article

References (51)

1. Devane, W. A., L. Hanus, A. Breuer, R. G. Pertwee, L. A. Stevenson, G. Griffin, D. Gibson, A. Mandelbaum, A. Etinger, and R. Mechoulam. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 258: 1946-1949. (Pubitemid 23026736)
2. Cravatt, B. F., D. K. Giang, S. P. Mayfield, D. L. Boger, R. A. Lerner, and N. B. Gilula. 1996. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature. 384: 83-87. (Pubitemid 26374593)
3. Cravatt, B. F., K. Demarest, M. P. Patricelli, M. H. Bracey, D. K. Giang, B. R. Martin, and A. H. Lichtman. 2001. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA. 98: 9371-9376. (Pubitemid 32743923)
4. Moreira, F. A., N. Kaiser, K. Monory, and B. Lutz. 2008. Reduced anxiety-like behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharm acol. 54: 141-150.
5. Aguado, T., K. Monory, J. Palazuelos, N. Stella, B. Cravatt, B. Lutz, G. Marsicano, Z. Kokaia, M. Guzmán, and I. Galve-Roperh. 2005. The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. FASEB J. 19: 1704-1706.
6. Cravatt, B. F., A. Saghatelian, E. G. Hawkins, A. B. Clement, M. H. Bracey, and A. H. Lichtman. 2004. Functional disassociation of the central and peripheral fatty acid amide signaling systems. Proc. Natl. Acad. Sci. USA. 101: 10821-10826. (Pubitemid 38955826)
7. Lichtman, A. H., C. C. Shelton, T. Advani, and B. F. Cravatt. 2004. Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain. 109: 319-327. (Pubitemid 38638709)
8. Boger, D. L., H. Sato, A. E. Lerner, M. P. Hedrick, R. A. Fecik, H. Miyauchi, G. D. Wilkie, B. J. Austin, M. P. Patricelli, and B. F. Cravatt. 2000. Exceptionally potent inhibitors of fatty acid amide hydrolase: The enzyme responsible for degradation of endogenous oleamide and anandamide. Proc. Natl. Acad. Sci. USA. 97: 5044-5049. (Pubitemid 30313668)
9. Kathuria, S., S. Gaetani, D. Fegley, F. Valiño, A. Duranti, A. Tontini, M. Mor, G. Tarzia, G. La Rana, A. Calignano, et al. 2003. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9: 76-81. (Pubitemid 36098263)
10. Boger, D. L., H. Miyauchi, W. Du, C. Hardouin, R. A. Fecik, H. Cheng, I. Hwang, M. P. Hedrick, D. Leung, O. Acevedo, et al. 2005. Discovery of a potent, selective, and efficacious class of reversible α-ketoheterocycle inhibitors of fatty acid amide hydrolase effective as analgesics. J. Med. Chem. 48: 1849-1856. (Pubitemid 40396316)
11. Keith, J. M., R. Apodaca, W. Xiao, M. Seierstad, K. Pattabiraman, J. Wu, M. Webb, M. J. Kabarz, S. Brown, S. Wilson, et al. 2008. Thiadiazolopiperazinyl ureas as inhibitors of fatty acid amide hydrolase. Bioorg. Med. Chem. Lett. 18: 4838-4843.
12. Berdyshev, E. V., P. C. Schmid, R. J. Kresbach, C. J. Hillard, C. Huang, N. Chen, Z. Dang, and H. O. Schmid. 2001. Cannabinoid-receptor- independent cell signaling by N -acylethanolamines. Biochem. J. 360: 67-75.
13. Dalle Carbonare, M., E. Del Giudice, A. Stecca, D. Colavito, M. Fabris, A. D'Arrigo, D. Bernardini, M. Dam, and A. Leon. 2008. A saturated N -acylethanolamine other than N -palmitoyl ethanolamine with anti-inflammatory properties: a neglected story.... J. Neuroendocrinol. 20 (Suppl. 1) : 26-34. (Pubitemid 351552673)
14. Tripathy, S., B. J. Venables, and K. D. Chapman. 1999. N-acylethanolamines in signal transduction of elicitor perception. Attenuation of alkalinization response and activation of defense gene expression. Plant Physiol. 121: 1299-1308. (Pubitemid 30018516)
15. Kang, L., Y-S. Wang, S. Uppalapati, K. Wang, Y. Tang, V. Vadapalli, B. J. Venables, K. D. Chapman, E. B. Blancaflor, and K. Mysore. 2008. Overexpression of a fatty acid amide hydrolase compromises innate immunity in Arabidopsis. Plant J. 56: 336-349.
16. Austin-Brown, S. L., and K. D. Chapman. 2002. Inhibition of phospholipase Dα by N-acylethanolamines. Plant Physiol. 129: 1892-1898.
17. Blancaflor, E. B., G. Hou, and K. D. Chapman. 2003. Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings. Planta. 217: 206-217. (Pubitemid 36796715)
18. Motes, C. M., P. Pechter, C. M. Yoo, Y. S. Wang, K. D. Chapman, and E. B. Blancaflor. 2005. Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth. Protoplasma. 226: 109-123. (Pubitemid 41752841)
19. Ellingson, J. S. 1980. Identification of (N-acyl)ethanolamine phosphoglycerides and acylphosphatidylglycerol as the phospholipids which disappear as Dictyostelium discoideum cells aggregate. Biochem istry. 19: 6176-6182.
20. Merkel, O., P. C. Schmid, F. Paltauf, and H. H. O. Schmid. 2005. Presence and potential signaling function of N -acylethanolamines and their phospholipids precursors in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1734: 215-219. (Pubitemid 40805078)
21. Anagnostopoulos, D., C. Rakiec, J. Wood, L. Pandarinathan, N. Zvonok, A. Makriyannis, and A. Siafaka-Kapadai. 2010. Identification of endocannabinoids and related N -acylethanolamines in Tetrahymena. A new class of compounds for Tetrahymena. Protist. 161: 452-465.
22. Karava, V., P-M. Zafiriou, L. Fasia, D. Anagnostopoulos, E. Boutou, C. E. Vorgias, M. Maccarrone, and A. Siafaka-Kapadai. 2005. Anandamide metabolism by Tetrahymena pyriformis in vitro. Characterization and identification of a 66 kDa fatty acid amidohydrolase. Biochimie. 87: 967-974. (Pubitemid 41377156)
23. 9- tetrahydrocannabinol on cell division and macromolecular synthesis in division-synchronized protozoa. Pharmacol. 14: 307-321.
24. 9 tetrahydrocannabinol on cyclic nucleotides in synchronously dividing Tetrahymena. Can. J. Biochem. 59: 489-493.
25. Dey, R., P. Pernin, and J. Bodennec. 2010. Endocannabinoids inhibit the growth of free-living amoebae. Antimicrob. Agents Chemother. 54: 3065-3067.
26. Schaloske, R. H., D. Blaesius, C. Schlatterer, and D. F. Lusche. 2007. Arachidonic acid is a chemoatttractant for Dictyostelium discoideum cells. J. Biosci. 32: 1281-1289.
27. Neelemagan, D., I. Schoenhofen, J. C. Richards, and A. D. Cox. 2012. Identification and recombinant expression of anadamide hydrolyzing enzyme from Dictyostelium discoideum. BMC Microbiol. 12: 124.
28. Williams, J., J. Wood, L. Pandarinathan, D. A. Karanian, B. A. Bahr, P. Vouros, and A. Makriyannis. 2007. Quantitative method for the profiling of the endocannabinoid metabolome by LCatmospheric pressure chemical ionization-MS. Anal. Chem. 79: 5582-5593. (Pubitemid 47229803)
29. McPartland, J. M., I. Matias, V. Di Marzo, and M. Glass. 2006. Evolutionary origins of the endocannabinoid system. Gene. 370: 64-74. (Pubitemid 43375901)
30. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948. (Pubitemid 350162903)
31. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. (Pubitemid 47236692)
32. Zoerner, A. A., S. Batkai, M-T. Suchy, F. M. Gutzki, S. Engeli, J. Jordan, and D. Tsikas. 2012. Simultaneous UPLC-MS/MS quantifi cation of the endocannabinoids 2-arachidonoyl glycerol (2AG), 1-arachidonoyl glycerol (1AG), and anandamide in human plasma: minimization of matrix-effects, 2AG/1AG isomerization and degradation by toluene solvent extraction. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 883-884: 161-171.
33. King, A. R., A. Duranti, A. Tontini, S. Rivara, A. Rosengarth, J. R. Clapper, G. Astarita, J. A. Geaga, H. Luecke, M. Mor, et al. 2007. URB602 inhibits monoacylglycerol lipase and selectivity blocks 2-arachidonoylglycerol degradation in intact brain slices. Chem. Biol. 14: 1357-1365. (Pubitemid 350257009)
34. Deutsch, D. G., R. Omeir, G. Arreaza, D. Salehani, G. D. Prestwich, Z. Huang, and A. Howlett. 1997. Methyl arachidonoyl fluorophosphonate: a potent irreversible inhibitor of anandamide amidase. Biochem. Pharmacol. 53: 255-260. (Pubitemid 27112941)
35. Alexander, J. P., and B. F. Cravatt. 2006. The putative endocannabinoid transport blocker LY2183240 is a potent inhibitor of FAAH and several other brain serine hydrolases. J. Am. Chem. Soc. 128: 9699-9704. (Pubitemid 44147953)
36. Boger, D. L., R. A. Fecik, J. E. Patterson, H. Miyauchi, M. P. Patricelli, and B. F. Cravatt. 2000. Fatty acid amide hydrolase susbstrate specificity. Bioorg. Med. Chem. Lett. 10: 2613-2616.
37. Shrestha, R., R. A. Dixon, and K. D. Chapman. 2003. Molecular identification of a functional homologue of the mammalian fatty acid amide hydrolase in Arabidopsis thaliana. J. Biol. Chem. 278: 34990-34997. (Pubitemid 37102260)
38. Bracey, M. H., M. A. Hanson, K. R. Masuda, R. C. Stevens, and B. F. Cravatt. 2002. Structural adaptations in a membrane enzyme that terminates endocannabiond signaling. Science. 298: 1793-1796. (Pubitemid 35404124)
39. McKinney, M. K., and B. F. Cravatt. 2003. Evidence for distinct roles in catalysis for residues of the serine-serine-lysine catalytic triad of fatty acid amide hydrolase. J. Biol. Chem. 278: 37393-37399. (Pubitemid 37175258)
40. Chapman, K. D., B. Venables, R. Blair, Jr., and C. Bettinger. 1999. N -acylethanolamines in seeds. Quantification of molecular species and their degradation upon imbibition. Plant Physiol. 120: 1157-1164. (Pubitemid 29411902)
41. Long, J. Z., M. LaCava, X. Jin, and B. F. Cravatt. 2011. An anatomical and temporal portrait of physiological substrates for fatty acid amide hydrolase. J. Lipid Res. 52: 337-344.
42. Keereetaweep, J., A. Kilaruna, I. Feussner, B. J. Venables, and K. D. Chapman. 2010. Lauroylethanolamide is a potent competitive inhibitor of lipoxygenase activity. FEBS Lett. 584: 3215-3222.
43. Devreotes, P. 1989. Dictyostelium discoideum: a model system for cellcell interactions in development. Science. 245: 1054-1058. (Pubitemid 19231812)
44. Francione, L. M., S. J. Anneslev, S. Carilla-Latorre, R. Escalante, and P. R. Fisher. 2011. The Dictyostelium model for mitochondrial disease. Semin. Cell Dev. Biol. 22: 120-130.
45. Meyer, I., O. Kuhnert, and R. Gräf. 2011. Functional analyses of lissencephaly-related proteins in Dictyostelium. Semin. Cell Dev. Biol. 22: 89-96.
46. Steinert, M., and K. Heuner. 2005. Dictyostelium as host model for pathogenesis. Cell. Microbiol. 7: 307-314. (Pubitemid 40277911)
47. Devreotes, P. N. 1988. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4: 649-686. (Pubitemid 19139268)
48. Kuhlmann, M., B. Popova, and W. Nellen. 2006. RNA interference and antisense-mediated gene silencing in Dictyostelium. In Dictyostelium discoideum protocols. Methods in molecular biology, Vol. 346. L. Eichinger and F. Rivero, editors. Humana Press, Totowa, NJ. 211-228.
49. Lambert, D. M., S. Vandevoorde, G. Diependaele, S. J. Govaerts, and A. R. Robert. 2001. Anticonvulsant activity of N -palmitoylethanolamide, a putative endocannabinoid, in mice. Epilpseia. 42: 321-327. (Pubitemid 32275910)
50. Maccarrone, M., R. Pauselli, M. Di Rienzo, and A. Finazzi-Agrò. 2002. Binding, degradation and apoptotic activity of stearoylethanolamide in rat C6 glioma cells. Biochem. J. 366: 137-144. (Pubitemid 34971812)
51. Fu, J., J. Kim, F. Oveisi, G. Astarita, and D. Piomelli. 2008. Targeted enhancement of oleoylethanolamide production in proximal small intestine induces across-meal satiety in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295: R45-R50.