Ketoconazole inhibits the cellular uptake of anandamide via inhibition of FAAH at pharmacologically relevant concentrations

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Björklund, Emmelie ^a   Larsson, Therése N L ^a   Jacobsson, Stig O P ^a   Fowler, Christopher J ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANANDAMIDE; FATTY ACID AMIDASE; KETOCONAZOLE; NEFAZODONE; QUINIDINE; SULFAPHENAZOLE;

ARTICLE; CACO 2 CELL LINE; CONTROLLED STUDY; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IC 50;

AMIDOHYDROLASES; ANALYSIS OF VARIANCE; ARACHIDONIC ACIDS; CACO-2 CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCANNABINOIDS; HEP G2 CELLS; HUMANS; KETOCONAZOLE; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB2;

EID: 84899788593     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087542     Document Type: Article

References (57)

1. Roques BP, Fournié-Zaluski MC, Wurm M (2012) Inhibiting the breakdown of endogenous opioids and cannabinoids to alleviate pain. Nat Rev Drug Discov 11: 292-310.
2. Di Marzo V, Ligresti A, Cristino L (2009) The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int J Obes (Lond) 33 Suppl 2: S18-24.
3. Battista N, Meccariello R, Cobellis G, Fasano S, Di Tommaso M, et al. (2012) The role of endocannabinoids in gonadal function and fertility along the evolutionary axis. Mol Cell Endocrinol 355: 1-14.
4. Idris AI, Ralston SH (2012) Role of cannabinoids in the regulation of bone remodeling. Front Endocrinol (Lausanne) 3: 136.
5. Pisanti S, Picardi P, D'Alessandro A, Laezza C, Bifulco M (2013) The endocannabinoid signaling system in cancer. Trends Pharmacol Sci 34: 273-282.
6. Fowler CJ (2013) Transport of endocannabinoids across the plasma membrane and within the cell. FEBS J 280: 1895-1904.
7. Kaczocha M, Glaser S, Deutsch D (2009) Identification of intracellular carriers for the endocannabinoid anandamide. Proc Natl Acad Sci USA 106: 6375-6380.
8. Oddi S, Fezza F, Pasquariello N, D'Agostino A, Catanzaro G, et al. (2009) Molecular identification of albumin and Hsp70 as cytosolic anandamide-binding proteins. Chem Biol 16: 624-632.
9. Fu J, Bottegoni G, Sasso O, Bertorelli R, Rocchia W, et al. (2011) A catalytically silent FAAH-1 variant drives anandamide transport in neurons. Nat Neurosci 15: 64-69.
10. Leung K, Elmes MW, Glaser ST, Deutsch DG, Kaczocha M (2013). Role of FAAH-like anandamide transporter in anandamide inactivation. PLoS One 8: e79355.
11. Deutsch DG, Chin SA (1993) Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem Pharmacol 46: 791-796. (Pubitemid 23272758)
12. Ueda N, Tsuboi K, Uyama T (2013) Metabolism of endocannabinoids and related N-acylethanolamines: Canonical and alternative pathways. FEBS J 280: 1874-1894.
13. Hermanson DJ, Hartley ND, Gamble-George J, Brown N, Shonesy BC, et al. (2013) Substrate-selective COX-2 inhibition decreases anxiety via endocannabinoid activation. Nat Neurosci 16: 1291-1298.
14. Gatta L, Piscitelli F, Giordano C, Boccella S, Lichtman A, et al. (2012) Discovery of prostamide F2a and its role in inflammatory pain and dorsal horn nociceptive neuron hyperexcitability. PLoS ONE 7: e31111.
15. Snider NT, Walker VJ, Hollenberg PF (2010) Oxidation of the endogenous cannabinoid arachidonoyl ethanolamide by the cytochrome p450 monooxygenases: physiological and pharmacological implications. Pharmacol Rev 62: 136-154.
16. Snider NT, Nast JA, Tesmer LA, Hollenberg PF (2009) A cytochrome P450-derived epoxygenated metabolite of anandamide is a potent cannabinoid receptor 2-selective agonist. Mol Pharmacol 75: 965-972.
17. Warrilow AG, Parker JE, Kelly DE, Kelly SL (2013) Azole affinity of sterol 14α-demethylase (CYP51) enzymes from Candida albicans and Homo sapiens. Antimicrob Agents Chemother 57: 1352-1360.
18. Sai Y, Dai R, Yang TJ, Krausz KW, Gonzalez FJ, et al. (2000) Assessment of specificity of eight chemical inhibitors using cDNA-expressed cytochromes P450. Xenobiotica 30: 327-343. (Pubitemid 30251243)
19. 17,20-lyase): potential agents for the treatment of prostatic cancer. J Med Chem 38: 2463-2471.
20. Beetens JR, Loots W, Somers Y, Coene MC, De Clerck F (1986) Ketoconazole inhibits the biosynthesis of leukotrienes in vitro and in vivo. Biochem Pharmacol 35: 883-891. (Pubitemid 16019848)
21. Rakhshan F, Day T, Blakeley R, Barker E (2000) Carrier-mediated uptake of the endogenous cannabinoid anandamide in RBL-2H3 cells. J Pharmacol Exp Ther 292: 960-967. (Pubitemid 30136588)
22. Sandberg A, Fowler CJ (2005) Measurement of saturable and non-saturable 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)
23. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
24. Boldrup L, Wilson SJ, Barbier AJ, Fowler CJ (2004) A simple stopped assay for fatty acid amide hydrolase avoiding the use of a chloroform extraction phase. J Biochem Biophys Methods 60: 171-177. (Pubitemid 38953060)
25. Beltramo M, Stella N, Calignano A, Lin SY, Makriyannis A, et al. (1997) Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277: 1094-1097. (Pubitemid 27371630)
26. Ortar G, Ligresti A, De Petrocellis L, Morera E, Di Marzo V (2003) Novel selective and metabolically stable inhibitors of anandamide cellular uptake. Biochem Pharmacol 65: 1473-1481. (Pubitemid 36559598)
27. Karlsson M, Påhlsson C, Fowler CJ (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)
28. Fowler CJ, Tiger G, Ligresti A, López-Rodriguez ML, 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)
29. Ortega-Gutiérrez S, Hawkins E, Viso A, López-Rodriguez M, Cravatt B (2004) Comparison of anandamide transport in FAAH wild-type and knockout neurons: evidence for contributions by both FAAH and the CB1 receptor to anandamide uptake. Biochemistry 43: 8184-8190. (Pubitemid 38808274)
30. Thors L, Fowler CJ (2006) Is there a temperature-dependent uptake of anandamide into cells? Br J Pharmacol 149: 73-81. (Pubitemid 44299070)
31. Kathuria S, Gaetani S, Fegley D, Valiño F, Duranti A, et al. (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9: 76-81. (Pubitemid 36098263)
32. Day T, Rakhshan F, Deutsch D, Barker E (2001) Role of fatty acid amide hydrolase in the transport of the endogenous canabinoid anandamide. Mol Pharmacol 59: 1369-1375. (Pubitemid 32510100)
33. Deutsch D, Glaser S, Howell J, Kunz J, Puffenbarger R, et al. (2001) The cellular uptake of anandamide is coupled to its breakdown by fatty-acid amide hydrolase. J Biol Chem 276: 6967-6973.
34. Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, et al. (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 5: 37-44.
35. Endsley M, Thill R, Choudhry I, Williams C, Kajdacsy-Balla A, et al. (2008) Expression and function of fatty acid amide hydrolase in prostate cancer. Int J Cancer 123: 1318-1326.
36. Thors L, Eriksson J, Fowler CJ (2007) Inhibition of the cellular uptake of anandamide by genistein and its analogue daidzein in cells with different levels of fatty acid amide hydrolase-driven uptake. Br J Pharmacol 152: 744-750. (Pubitemid 350034971)
37. Vandevoorde S, Jonsson K-O, Fowler CJ, Lambert DM (2003). Modifications of the ethanolamine head in N-palmitoylethanolamine: synthesis and evaluation of new agents interfering with the metabolism of anandamide. J Med Chem 46: 1440-1448. (Pubitemid 36512706)
38. Tolman EL, Fuller BL (1983) Inhibition of thromboxane synthesis in guinea pig lung and human platelets by clotrimazole and other imidazole antifungals. Biochem Pharmacol 32:3488-3490. (Pubitemid 14203709)
39. Lelcuk S, Huval WV, Valeri CR, Shepro D, Hechtman HB (1984) Inhibition of ischemia-induced thromboxane synthesis in man. J Trauma 24:393-396. (Pubitemid 14101802)
40. Sekar VJ, Lefebvre E, De Pauw M, Vangeneugden T, Hoetelmans RM (2008) Pharmacokinetics of darunavir/ritonavir and ketoconazole following coadministration in HIV-healthy volunteers. Br J Clin Pharmacol 66: 215-221.
41. Hillard C, Jarrahian A (2005) Accumulation of anandamide: evidence for cellular diversity. Neuropharmacology 48: 1072-1078. (Pubitemid 40725979)
42. Beltramo M, Piomelli D (2000) Carrier-mediated transport and enzymatic hydrolysis of the endogenous cannabinoid 2-arachidonylglycerol. NeuroReport 11: 1231-1235. (Pubitemid 30262964)
43. Fowler CJ, Ghafouri N (2008). Does the hydrolysis of 2- arachidonoylglycerol regulate its cellular uptake? Pharmacol Res 58: 72-76.
44. Chicca A, Marazzi J, Nicolussi S, Gertsch J (2012). Evidence for bidirectional endocannabinoid transport across cell membranes. J Biol Chem 287: 34660-34682.
45. Chen Y, Falck JR, Manthati VL, Jat JL, Campbell WB (2011) 20-Iodo-14,15-epoxyeicosa-8(Z)-enoyl-3-azidophenylsulfonamide: photoaffinity labeling of a 14,15-epoxyeicosatrienoic acid receptor. Biochemistry 50: 3840-3848.
46. Tölle A, Suhail S, Jung M, Jung K, Stephan C (2011) Fatty acid binding proteins (FABPs) in prostate, bladder and kidney cancer cell lines and the use of IL-FABP as survival predictor in patients with renal cell carcinoma. BMC Cancer 11: 302.
47. Freimuth N, Ramer R, Hinz B (2010) Antitumorigenic effects of cannabinoids beyond apoptosis. J Pharmacol Exp Ther 332: 336-344.
48. Fowler CJ, Gustafsson SB, Chung SC, Persson E, Jacobsson SOP, et al. (2010) Targeting the endocannabinoid system for the treatment of cancer - a practical view. Curr Top Med Chem 10: 814-827.
49. Diaz-Laviada I (2011) The endocannabinoid system in prostate cancer. Nat Rev Urol 8: 553-561.
50. Guindon J, Hohmann AG (2011) The endocannabinoid system and cancer: therapeutic implication. Br J Pharmacol 163: 1447-1463.
51. Velasco G, Sanchez C, Guzmán M (2012) Towards the use of cannabinoids as antitumour agents. Nat Rev Cancer 12: 436-444.
52. Worthington HV, Clarkson JE, Khalid T, Meyer S, McCabe M (2010) Interventions for treating oral candidiasis for patients with cancer receiving treatment. Cochrane Database Syst Rev 2010: CD001972.
53. Zee YK, Goh BC, Lee SC (2012) Pharmacologic modulation strategies to reduce dose requirements of anticancer therapy while preserving clinical efficacy. Future Oncol 8:731-749.
54. Vasaitis TS, Bruno RD, Njar VC (2011) CYP17 inhibitors for prostate cancer therapy. J Steroid Biochem Mol Biol 125: 23-31.
55. Morphy R, Rankovic Z (2005) Designed multiple ligands. An emerging drug discovery paradigm. J Med Chem 48: 6523-6543. (Pubitemid 41504710)
56. Starowicz K, Di Marzo V (2013) Non-psychotropic analgesic drugs from the endocannabinoid system: "magic bullet" or "multiple-target" strategies? Eur J Pharmacol 716: 41-53.
57. Fowler CJ, Naidu PS, Lichtman A, Onnis V (2009) The case for the development of novel analgesic agents targeting both fatty acid amide hydrolase and either cyclooxygenase or TRPV1. Br J Pharmacol 156: 412-419.