Selective inhibition of anandamide cellular uptake versus enzymatic hydrolysis - A difficult issue to handle

European Journal of Pharmacology

Volumn 492, Issue 1, 2004, Pages 1-11

  Fowler, Christopher J ^a   Tiger, Gunnar ^a   Ligresti, Alessia ^b   López Rodríguez, María L ^c   Di Marzo, Vincenzo ^b  

^a UMEÅ UNIVERSITY   (Sweden)

^b CNR   (Italy)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Anandamide uptake; C6 glioma cell; Endocannabinoid; Fatty acid amide hydrolase

Indexed keywords

AMIDE; ANANDAMIDE; ENZYME INHIBITOR; FATTY ACID AMIDASE; N (3 FURYLMETHYL)ARACHIDONAMIDE; N (4 HYDROXY 2 METHYLPHENYL)ARACHIDONAMIDE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRAIN U937; CELL TYPE; CONTROLLED STUDY; DRUG EFFECT; DRUG UPTAKE; ENANTIOMER; ENZYME ASSAY; GLIOMA CELL; HUMAN; HUMAN CELL; HYDROLYSIS; IC 50; LEUKEMIA CELL LINE; MAST CELL LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; RAT; SPECIES;

ADSORPTION; AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BENZYL COMPOUNDS; BIOLOGICAL TRANSPORT; BRAIN; ENZYME INHIBITORS; FURANS; HUMANS; HYDROLYSIS; MICE; POLYUNSATURATED ALKAMIDES; RATS; RATS, SPRAGUE-DAWLEY; TUMOR CELLS, CULTURED;

EID: 2442595984     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2004.03.048     Document Type: Article

References (50)

1. Basavarajappa B.S., Saito M., Cooper T.B., Hungund B.L. Chronic ethanol inhibits the anandamide transport and increases extracellular anandamide levels in cerebellar granule neurons. Eur. J. Pharmacol. 466:2003;73-83
2. Beltramo M., Stella N., Calignano A., Lin S.Y., Makriyannis A., Piomelli D. Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science. 277:1997;1094-1097
3. Bisogno T., Maurelli S., Melck D., De Petrocellis L., Di Marzo V. Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J. Biol. Chem. 272:1997;3315-3323
4. Bisogno T., Maccarrone M., De Petrocellis L., Jarrahian A., Finazzi-Agró A., Hillard C., Di Marzo V. The uptake by cells of 2-arachidonoylglycerol, an endogenous agonist of cannabinoid receptors. Eur. J. Biochem. 268:2001;1982-1989
5. Biswas K.K., Sarker K.P., Abeyama K., Kawahara K.-I., Iino S., Otsubo Y., Saigo H., Hashiguchi T., Yamkuchi M., Yamaji K., Endo R., Suzuki K., Imaizumi H., Maruyama I. Membrane cholesterol but not putative receptors mediates anandamide-induced hepatocyte apoptosis. Hepatology. 38:2003;1167-1177
6. Bloom A.S., Edgemond W.S., Moldvan J.C. Nonclassical and endogenous cannabinoids: effects on the ordering of brain membranes. Neurochem. Res. 22:1997;563-568
7. Bojesen I.N., Hansen H.S. Binding of anandamide to bovine serum albumin. J. Lipid Res. 44:2003;1790-1794
8. Cadas H., Schinelli S., Piomelli D. Membrane localization of N-acylphosphatidylethanolamine in central neurons: studies with exogenous phospholipases. J. Lipid Mediators Cell Signal. 14:1996;63-70
9. 2+, questioning its selectivity as a pharmacological tool for investigating the anandamide transporter. J. Pharmacol. Toxicol. Methods. 45:2001;195-198
10. Day T.A., Rakhshan F., Deutsch D.G., Barker E.L. Role of fatty acid amide hydrolase in the transport of the endogenous cannabinoid anandamide. Mol. Pharmacol. 59:2001;1369-1375
11. De Petrocellis L., Bisogno T., Davis J.B., Pertwee R.G., Di Marzo V. Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide uptake with negligible capsaicin-like activity. FEBS Lett. 483:2000;52-56
12. De Petrocellis L., Davis J.B., Di Marzo V. Palmitoylethanolamide enhances anandamide stimulation of human vanilloid VR1 receptors. FEBS Lett. 506:2001;253-256
13. Deutsch D.G., Chin S.A. Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem. Pharmacol. 46:1993;791-797
14. Deutsch D.G., Glaser S.T., Howell J.M., Kunz J.S., Puffenbarger R.A., Hillard C.J., Abumrad N. The cellular uptake of anandamide is coupled to its breakdown by fatty acid amide hydrolase (FAAH). J. Biol. Chem. 276:2001;6967-6973
15. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J.C., Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature. 372:1994;686-691
16. Di Marzo V., Bisogno T., De Petrocellis L., Brandi I., Jefferson R.G., Winckler R.L., Davis J.B., Dasse O., Mahadevan A., Razdan R.K., Martin B.R. Highly selective CB1 cannabinoid receptor ligands and novel CB1/VR1 vanilloid receptor "hybrid" ligands. Biochem. Biophys. Res. Commun. 281:2001;444-451
17. 3H]anandamide by rabbit platelets. Lack of transporter? Eur. J. Biochem. 270:2003;3498-3506
18. Fowler C.J., Brännstrom G. Reduction in beta-adrenoceptor density in cultured rat glioma C6 cells after incubation with antidepressants is dependent upon the culturing conditions used. J. Neurochem. 55:1990;245-250
19. Karlsson, M., Påhlsson, C., Fowler, C.J., Reversible, temperature-dependent, and AM404-inhibitable adsorption of anandamide to cell culture wells as a confounding factor in release experiments. Eur. J. Pharm. Sci., in press.
20. Fowler C.J., Jonsson K.-O., Tiger G. Fatty acid amide hydrolase: biochemistry, pharmacology, and therapeutic possibilities for an enzyme hydrolyzing anandamide, 2-arachidonoylglycerol, palmitoylethanolamide, and oleamide. Biochem. Pharmacol. 62:2001;517-526
21. Fowler C.J., Holt S., Tiger G. Acidic nonsteroidal anti-inflammatory drugs inhibit rat brain fatty acid amide hydrolase in a pH-dependent manner. J. Enzyme Inhib. Med. Chem. 18:2003;55-58
22. Glaser S., Abumrad N., Fatade F., Kaczocha M., Studholme K., Deutsch D. Evidence against the presence of an anandamide transporter. Proc. Natl. Acad. Sci. U. S. A. 100:2003;4269-4274
23. Gubits R.M., Yu H., Casey G., Munell F., Vitek M.P. Altered genetic response to beta-adrenergic receptor activation in late passage C6 glioma cells. J. Neurosci. Res. 33:1992;297-305
24. Harrington C.R. Lowry protein assay containing sodium dodecyl sulfate in microtiter plates for protein determination on fractions from brain tissue. Anal. Biochem. 186:1990;285-287
25. Hillard C.J., Jarrahian A. The movement of N-arachidonoylethanolamine (anandamide) across cellular membranes. Chem. Phys. Lipids. 108:2000;123-134
26. Hillard C.J., Jarrahian A. Cellular accumulation of anandamide: consensus and controversy. Br. J. Pharmacol. 140:2003;802-808
27. Hillard C.J., Wilkison D.M., Edgemond W.S., Campbell W.B. Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. Biochim. Biophys. Acta. 1257:1995;249-256
28. Hillard C.J., Edgemond W.S., Jarrahian A., Campbell W.B. Accumulation of N-arachidonoylethanolamine (anandamide) into cerebellar granule cells occurs via facilitated diffusion. J. Neurochem. 69:1997;631-638
29. Holt S., Fowler C.J. Anandamide metabolism by fatty acid amide hydrolase in intact C6 glioma cells. Increased sensitivity to inhibition by ibuprofen and flurbiprofen upon reduction of extra - but not intracellular pH. Naunyn-Schmiedeberg's Arch. Pharmacol. 367:2003;237-244
30. Holt S., Nilsson J., Omeir R., Tiger G., Fowler C.J. Effects of pH on the inhibition of fatty acid amidohydrolase by ibuprofen. Br. J. Pharmacol. 133:2001;513-520. (Corrigendum published in Br. J. Pharmacol., 134, 451)
31. Jacobsson S.O.P., Fowler C.J. Characterization of palmitoylethanolamide transport in mouse Neuro-2a neuroblastoma and rat RBL-2H3 basophilic leukaemia cells: comparison with anandamide. Br. J. Pharmacol. 132:2001;1743-1754
32. Jacobsson S.O.P., Wallin T., Fowler C.J. Inhibition of rat C6 glioma cell proliferation by endogenous and synthetic cannabinoids. Relative involvement of cannabinoid and vanilloid receptors. J. Pharmacol. Exp. Ther. 299:2001;951-959
33. Jarrahian A., Manna S., Edgemond W.S., Campbell W.B., Hillard C.J. Structure-activity relationships among N-arachidonoylethanolamine (anandamide) head group analogues for the anandamide transported. J. Neurochem. 74:2000;2597-2606
34. Jonsson K.-O., Vandevoorde S., Lambert D.M., Tiger G., Fowler C.J. Effects of homologues and analogues of palmitoylethanolamide upon the inactivation of the endocannabinoid anandamide. Br. J. Pharmacol. 133:2001;1263-1275
35. Jonsson K.-O., Andersson A., Jacobsson S.O.P., Vandevoorde S., Lambert D.M., Fowler C.J. AM404 and VDM 11 non-specifically inhibit C6 glioma cell proliferation at concentrations used to block the cellular accumulation of the endocannabinoid anandamide. Arch. Toxicol. 77:2003;201-207
36. Kathuria S., Gaetani S., Fegley D., Valiño F., Duranti A., Tontini A., Mor M., Tarzia G., La Rana G., Calignano A., Giustino A., Tattoli M., Palmery M., Cuomo V., Piomelli D. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9:2003;76-81
37. Ligresti A., Morera E., van der Stelt M., Monory K., Lutz B., Ortar G., Di Marzo V. Further evidence for the existence of a specific process for the membrane transport of anandamide. Biochem. J. 2004;. (in press)
38. López-Rodríguez M.L., Viso A., Ortega-Gutiérrez S., Fowler C.J., Tiger G., de Lago E., Fernández-Ruiz J., Ramos J.A. Design, synthesis and biological evaluation of new endocannabinoid transporter inhibitors: comparison with effects upon fatty acid amidohydrolase. J. Med. Chem. 46:2003;1512-1522
39. Maurelli S., Bisogno T., De Petrocellis L., Di Luccia A., Marino G., Di Marzo V. Two novel classes of neuroactive fatty acid amides are substrates for mouse neuroblastoma 'anandamide amidohydrolase'. FEBS Lett. 377:1995;82-86
40. McFarland M.J., Porter A.C., Barker E.L. Uptake of the endogenous cannabinoid anandamide by endocytic processes and accumulation in lipid rafts. Exp. Biol. 2003;. (Abstract #3718, http://www.biosis-select.org/faseb/data/ FASEB003718.html)
41. Okamoto Y., Morishita J., Tsuboi K., Tonai T., Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J. Biol. Chem. 279:2004;5298-5305
42. 14C] as a substrate for anandamide amidase. Life Sci. 56:1995;1999-2005
43. Ortar G., Ligresti A., De Petrocellis L., Morera E., Di Marzo V. Novel selective and metabolically stable inhibitors of anandamide cellular uptake. Biochem. Pharmacol. 65:2003;1473-1481
44. Rakhshan F., Day T.A., Blakely R.D., Barker E.L. Carrier-mediated uptake of the endogenous cannabinoid anandamide in RBL-2H3 cells. J. Pharmacol. Exp. Ther. 292:2000;960-967
45. Ruiz-Llorente L., Ortega-Gutiérrez S., Viso A., Sánchez M.G., Sánchez A.M., Fernández C., Ramos J.A., Hillard C., Lasunción M.A., López-Rodríguez M.L., Díaz-Laviada I. Characterization of an anandamide degradation system in prostate epithelial PC-3 cells: synthesis of new transporter inhibitors as tools for this study. Br. J. Pharmacol. 141:2004;457-467
46. Sarker K.P., Maruyama I. Anandamide induces cell death independently of cannabinoid receptors or vanilloid receptor 1: possible involvement of lipid rafts. Cell. Mol. Life Sci. 60:2003;1200-1208
47. Schmid P.C., Reddy P.V., Natarajan V., Schmid H.H.O. Metabolism of N-acylethanolamine phospholipids by a mammalian phosphodiesterase of the phospholipase D type. J. Biol. Chem. 258:1983;9302-9306
48. Schmid P.C., Zuzarte-Augustin M.L., Schmid H.H.O. Properties of rat liver N-acylethanolamine amidohydrolase. J. Biol. Chem. 260:1985;14145-14149
49. Vandevoorde S., Jonsson K.-O., Fowler C.J., Lambert D.M. Modifications of the ethanolamine head in N-palmitoylethanolamine: synthesis and evaluation of new agents interfering with the metabolism of anandamide. J. Med. Chem. 46:2003;1440-1448
50. Wilson S.J., Lovenberg T.W., Barbier A.J. A high-throughput-compatible assay for determining the activity of fatty acid amide hydrolase. Anal. Biochem. 318:2003;270-275