Fatty acid-binding proteins transport N-acylethanolamines to nuclear receptors and are targets of endocannabinoid transport inhibitors

Journal of Biological Chemistry

Volumn 287, Issue 5, 2012, Pages 3415-3424

  Kaczocha, Martin ^a   Vivieca, Stephanie ^a   Sun, Jing ^a   Glaser, Sherrye T ^b   Deutsch, Dale G ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b KINGSBOROUGH COMMUNITY COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOACTIVE LIPIDS; CELLULAR TARGETS; CHEMICAL INHIBITION; ENDOCANNABINOID; FATTY ACID-BINDING PROTEINS; IN-VITRO; N-ACYLETHANOLAMINES; NUCLEAR RECEPTORS; NUCLEAR TRANSLOCATIONS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PHARMACOLOGICAL INHIBITION; PHYSIOLOGICAL EFFECTS; RECEPTOR SYSTEM; TRANSMEMBRANES; TRANSPORT INHIBITORS;

CYTOLOGY; TRANSCRIPTION FACTORS;

FATTY ACIDS;

ENDOCANNABINOID; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 3; FATTY ACID BINDING PROTEIN 5; FATTY ACID BINDING PROTEIN 7; LIPID; N ACYLETHANOLAMINE; N OLEOYLETHANOLAMINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; IN VITRO STUDY; MEMBRANE TRANSPORT; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; ENDOCANNABINOIDS; ETHANOLAMINES; FATTY ACID-BINDING PROTEINS; HELA CELLS; HUMANS; MICE; OLEIC ACIDS; PPAR ALPHA; SIGNAL TRANSDUCTION;

EID: 84863012327     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.304907     Document Type: Article

References (59)

1. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., and Mechoulam, R. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949 (Pubitemid 23026736)
2. Fu, J., Gaetani, S., Oveisi, F., Lo Verme, J., Serrano, A., Rodríguez De Fonseca, F., Rosengarth, A., Luecke, H., Di Giacomo, B., Tarzia, G., and Piomelli, D. (2003) Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-α. Nature 425, 90-93 (Pubitemid 37101723)
3. Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., and Piomelli, D. (2005) The nuclear receptor peroxisome proliferator- activated receptor-α mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19 (Pubitemid 40069962)
4. Cravatt, B. F., Demarest, K., Patricelli, M. P., Bracey, M. H., Giang, D. K., Martin, B. R., and Lichtman, A. H. (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. U.S.A. 98, 9371-9376 (Pubitemid 32743923)
5. Lichtman, A. H., Shelton, C. C., Advani, T., and Cravatt, B. F. (2004) Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain 109, 319-327 (Pubitemid 38638709)
6. Kaczocha, M., Glaser, S. T., and Deutsch, D. G. (2009) Identification of intracellular carriers for the endocannabinoid anandamide. Proc. Natl. Acad. Sci. U.S.A. 106, 6375-6380
7. Glaser, S. T., Abumrad, N. A., Fatade, F., Kaczocha, M., Studholme, K. M., and Deutsch, D. G. (2003) Evidence against the presence of an anandamide transporter. Proc. Natl. Acad. Sci. U.S.A. 100, 4269-4274 (Pubitemid 36418192)
8. Kaczocha, M., Hermann, A., Glaser, S. T., Bojesen, I. N., and Deutsch, D. G. (2006) Anandamide uptake is consistent with rate-limited diffusion and is regulated by the degree of its hydrolysis by fatty acid amide hydrolase. J. Biol. Chem. 281, 9066-9075 (Pubitemid 43864619)
9. 3H]anandamide by rabbit platelets. Lack of transporter? Eur. J. Biochem. 270, 3498-3506
10. Bojesen, I. N., and Hansen, H. S. (2005) Membrane transport of anandamide through resealed human red blood cell membranes. J. Lipid Res. 46, 1652-1659 (Pubitemid 41099332)
11. Sandberg, A., and Fowler, C. J. (2005) Measurement of saturable and nonsaturable components of anandamide uptake into P19 embryonic carcinoma cells in the presence of fatty acid-free bovine serum albumin. Chem. Phys. Lipids 134, 131-139 (Pubitemid 40387392)
12. Beltramo, M., Stella, N., Calignano, A., Lin, S. Y., Makriyannis, A., and Piomelli, D. (1997) Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277, 1094-1097 (Pubitemid 27371630)
13. Piomelli, D., Beltramo, M., Glasnapp, S., Lin, S. Y., Goutopoulos, A., Xie, X. Q., and Makriyannis, A. (1999) Structural determinants for recognition and translocation by the anandamide transporter. Proc. Natl. Acad. Sci. U.S.A. 96, 5802-5807 (Pubitemid 29234699)
14. Ortar, G., Ligresti, A., De Petrocellis, L., Morera, E., and Di Marzo, V. (2003) Novel selective and metabolically stable inhibitors of anandamide cellular uptake. Biochem. Pharmacol. 65, 1473-1481 (Pubitemid 36559598)
15. Fegley, D., Kathuria, S., Mercier, R., Li, C., Goutopoulos, A., Makriyannis, A., and Piomelli, D. (2004) Anandamide transport is independent of fatty acid amide hydrolase activity and is blocked by the hydrolysis-resistant inhibitor AM1172. Proc. Natl. Acad. Sci. U.S.A. 101, 8756-8761 (Pubitemid 38745844)
16. Hasanein, P. (2009) The endocannabinoid transport inhibitor AM404 modulates nociception in cholestasis. Neurosci. Lett. 462, 230-234
17. La Rana, G., Russo, R., D'Agostino, G., Sasso, O., Raso, G. M., Iacono, A., Meli, R., Piomelli, D., and Calignano, A. (2008) AM404, an anandamide transport inhibitor, reduces plasma extravasation in a model of neuropathic pain in rat. Role for cannabinoid receptors. Neuropharmacology 54, 521-529
18. Adermark, L., Talani, G., and Lovinger, D. M. (2009) Endocannabinoid- dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur. J. Neurosci. 29, 32-41
19. Ronesi, J., Gerdeman, G. L., and Lovinger, D. M. (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J. Neurosci. 24, 1673-1679 (Pubitemid 38240964)
20. Adermark, L., and Lovinger, D. M. (2007) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc. Natl. Acad. Sci. U.S.A. 104, 20564-20569
21. Glaser, S. T., and Kaczocha, M. (2010) Cyclooxygenase-2 mediates anandamide metabolism in the mouse brain. J. Pharmacol. Exp. Ther. 335, 380-388
22. Schug, T. T., Berry, D. C., Shaw, N. S., Travis, S. N., and Noy, N. (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129, 723-733 (Pubitemid 46802374)
23. Tan, N. S., Shaw, N. S., Vinckenbosch, N., Liu, P., Yasmin, R., Desvergne, B., Wahli, W., and Noy, N. (2002) Selective cooperation between fatty acid-binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol. Cell Biol. 22, 5114-5127 (Pubitemid 34700702)
24. Day, T. A., Rakhshan, F., Deutsch, D. G., and Barker, E. L. (2001) Role of fatty acid amide hydrolase in the transport of the endogenous cannabinoid anandamide. Mol. Pharmacol. 59, 1369-1375 (Pubitemid 32510100)
25. Kaczocha, M., Glaser, S. T., Chae, J., Brown, D. A., and Deutsch, D. G. (2010) Lipid droplets are novel sites of N-acylethanolamine inactivation by fatty acid amide hydrolase-2. J. Biol. Chem. 285, 2796-2806
26. Ziouzenkova, O., Perrey, S., Asatryan, L., Hwang, J., MacNaul, K. L., Moller, D. E., Rader, D. J., Sevanian, A., Zechner, R., Hoefler, G., and Plutzky, J. (2003) Lipolysis of triglyceride-rich lipoproteins generates PPAR ligands. Evidence for an anti-inflammatory role for lipoprotein lipase. Proc. Natl. Acad. Sci. U.S.A. 100, 2730-2735 (Pubitemid 36297567)
27. Furuhashi, M., Tuncman, G., Görgün, C. Z., Makowski, L., Atsumi, G., Vaillancourt, E., Kono, K., Babaev, V. R., Fazio, S., Linton, M. F., Sulsky, R., Robl, J. A., Parker, R. A., and Hotamisligil, G. S. (2007) Treatment of diabetes and atherosclerosis by inhibiting fatty acid-binding protein aP2. Nature 447, 959-965 (Pubitemid 46975747)
28. De Petrocellis, L., Bisogno, T., Davis, J. B., Pertwee, R. G., and Di Marzo, V. (2000) 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, 52-56
29. Deutsch, D. G., Glaser, S. T., Howell, J. M., Kunz, J. S., Puffenbarger, R. A., Hillard, C. J., and Abumrad, N. (2001) The cellular uptake of anandamide is coupled to its breakdown by fatty acid amide hydrolase. J. Biol. Chem. 276, 6967-6973
30. Vandevoorde, S., and Fowler, C. J. (2005) Inhibition of fatty acid amide hydrolase and monoacylglycerol lipase by the anandamide uptake inhibitor VDM11. Evidence that VDM11 acts as an FAAH substrate. Br. J. Pharmacol. 145, 885-893 (Pubitemid 41129010)
31. Howlett, A. C., Reggio, P. H., Childers, S. R., Hampson, R. E., Ulloa, N. M., and Deutsch, D. G. (2011) Endocannabinoid tone versus constitutive activity of cannabinoid receptors. Br. J. Pharmacol. 163, 1329-1343
32. Chuang, S., Velkov, T., Horne, J., Porter, C. J., and Scanlon, M. J. (2008) Characterization of the drug binding specificity of rat liver fatty acidbinding protein. J. Med. Chem. 51, 3755-3764 (Pubitemid 351956507)
33. Wolfrum, C. (2007) Cytoplasmic fatty acid-binding protein sensing fatty acids for peroxisome proliferator-activated receptor activation. Cell. Mol. Life Sci. 64, 2465-2476
34. Richieri, G. V., Ogata, R. T., Zimmerman, A. W., Veerkamp, J. H., and Kleinfeld, A. M. (2000) Fatty acid-binding proteins from different tissues show distinct patterns of fatty acid interactions. Biochemistry 39, 7197-7204 (Pubitemid 30413109)
35. Xu, L. Z., Sánchez, R., Sali, A., and Heintz, N. (1996) Ligand specificity of brain lipid-binding protein. J. Biol. Chem. 271, 24711-24719 (Pubitemid 26333215)
36. Mallet, C., Barriere, D. A., Ermund, A., Jonsson, B. A., Eschalier, A., Zygmunt, P. M., and Hogestatt, E. D. (2010) PLoS One 5, e12748
37. Högestätt, E. D., Jönsson, B. A., Ermund, A., Andersson, D. A., Björk, H., Alexander, J. P., Cravatt, B. F., Basbaum, A. I., and Zygmunt, P. M. (2005) Conversion of acetaminophen to the bioactive N-acylphenolamine AM404 via fatty acid amide hydrolase-dependent arachidonic acid conjugation in the nervous system. J. Biol. Chem. 280, 31405-31412 (Pubitemid 41291881)
38. Oddi, S., Fezza, F., Pasquariello, N., D'Agostino, A., Catanzaro, G., De Simone, C., Rapino, C., Finazzi-Agrò, A., and Maccarrone, M. (2009) Molecular identification of albumin and Hsp70 as cytosolic anandamide-binding proteins. Chem. Biol. 16, 624-632
39. Glaser, S. T., Kaczocha, M., and Deutsch, D. G. (2005) Anandamide transport. A critical review. Life Sci. 77, 1584-1604
40. McFarland, M. J., and Barker, E. L. (2004) Anandamide transport. Pharmacol. Ther. 104, 117-135 (Pubitemid 39424256)
41. Thors, L., and Fowler, C. J. (2006) Is there a temperature-dependent uptake of anandamide into cells? Br. J. Pharmacol. 149, 73-81 (Pubitemid 44299070)
42. Fowler, C. J., Tiger, G., Ligresti, A., López-Rodríguez, M. L., and Di Marzo, V. (2004) Selective inhibition of anandamide cellular uptake versus enzymatic hydrolysis, a difficult issue to handle. Eur. J. Pharmacol. 492, 1-11 (Pubitemid 38624415)
43. Karlsson, M., Påhlsson, C., and Fowler, C. J. (2004) Reversible, temperature-dependent, and AM404-inhibitable adsorption of anandamide to cell culture wells as a confounding factor in release experiments. Eur. J. Pharm. Sci. 22, 181-189 (Pubitemid 38668683)
44. Furuhashi, M., and Hotamisligil, G. S. (2008) Fatty acid-binding proteins. Role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 7, 489-503 (Pubitemid 351767117)
45. Owada, Y., Yoshimoto, T., and Kondo, H. (1996) Spatio-temporally differential expression of genes for three members of fatty acid-binding proteins in developing and mature rat brains. J. Chem. Neuroanat. 12, 113-122 (Pubitemid 27056799)
46. Fezza, F., Oddi, S., Di Tommaso, M., De Simone, C., Rapino, C., Pasquariello, N., Dainese, E., Finazzi-Agrò, A., and Maccarrone, M. (2008) Characterization of biotin-anandamide, a novel tool for the visualization of anandamide accumulation. J. Lipid Res. 49, 1216-1223
47. Oddi, S., Bari, M., Battista, N., Barsacchi, D., Cozzani, I., and Maccarrone, M. (2005) Confocal microscopy and biochemical analysis reveal spatial and functional separation between anandamide uptake and hydrolysis in human keratinocytes. Cell. Mol. Life Sci. 62, 386-395 (Pubitemid 40379252)
48. Fu, J., Bottegoni, G., Sasso, O., Bertorelli, R., Rocchia, W., Masetti, M., Guijarro, A., Lodola, A., Armirotti, A., Garau, G., Bandiera, T., Reggiani, A., Mor, M., Cavalli, A., and Piomelli, D. (2012) Nat. Neurosci. 15, 64-69
49. Kim, J., and Alger, B. E. (2010) Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat. Neurosci. 13, 592-600
50. Spradley, J. M., Guindon, J., and Hohmann, A. G. (2010) Inhibitors of monoacylglycerol lipase, fatty-acid amide hydrolase and endocannabinoid transport differentially suppress capsaicin-induced behavioral sensitization through peripheral endocannabinoid mechanisms. Pharmacol. Res. 62, 249-258
51. La Rana, G., Russo, R., Campolongo, P., Bortolato, M., Mangieri, R. A., Cuomo, V., Iacono, A., Raso, G. M., Meli, R., Piomelli, D., and Calignano, A. (2006) Modulation of neuropathic and inflammatory pain by the endocannabinoid transport inhibitor AM404 (N-(4-hydroxyphenyl)-eicosa-5,8,11,14-tetraenamide). J. Pharmacol. Exp. Ther. 317, 1365-1371 (Pubitemid 43764143)
52. Zygmunt, P. M., Chuang, H., Movahed, P., Julius, D., and Högestätt, E. D. (2000) The anandamide transport inhibitor AM404 activates vanilloid receptors. Eur. J. Pharmacol. 396, 39-42 (Pubitemid 30261557)
53. Nicholson, R. A., Liao, C., Zheng, J., David, L. S., Coyne, L., Errington, A. C., Singh, G., and Lees, G. (2003) Sodium channel inhibition by anandamide and synthetic cannabimimetics in brain. Brain Res. 978, 194-204 (Pubitemid 36776639)
54. Kelley, B. G., and Thayer, S. A. (2004) Anandamide transport inhibitor AM404 and structurally related compounds inhibit synaptic transmission between rat hippocampal neurons in culture independent of cannabinoid CB1 receptors. Eur. J. Pharmacol. 496, 33-39 (Pubitemid 39024313)
55. Alptekin, A., Galadari, S., Shuba, Y., Petroianu, G., and Oz, M. (2010) The effects of anandamide transport inhibitor AM404 on voltage-dependent calcium channels. Eur. J. Pharmacol. 634, 10-15
56. Trezza, V., and Vanderschuren, L. J. (2009) Divergent effects of anandamide transporter inhibitors with different target selectivity on social play behavior in adolescent rats. J. Pharmacol. Exp. Ther. 328, 343-350
57. Lastres-Becker, I., de Miguel, R., De Petrocellis, L., Makriyannis, A., Di Marzo, V., and Fernández-Ruiz, J. (2003) Compounds acting at the endocannabinoid and/or endovanilloid systems reduce hyperkinesia in a rat model of Huntington disease. J. Neurochem. 84, 1097-1109 (Pubitemid 36330662)
58. Sagar, D. R., Jhaveri, M. D., Richardson, D., Gray, R. A., de Lago, E., Fernández-Ruiz, J., Barrett, D. A., Kendall, D. A., and Chapman, V. (2010) Endocannabinoid regulation of spinal nociceptive processing in a model of neuropathic pain. Eur. J. Neurosci. 31, 1414-1422
59. Erbay, E., Babaev, V. R., Mayers, J. R., Makowski, L., Charles, K. N., Snitow, M. E., Fazio, S., Wiest, M. M., Watkins, S. M., Linton, M. F., and Hotamisligil, G. S. (2009) Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis. Nat. Med. 15, 1383-1391