Anandamide and its congeners inhibit human plasma butyrylcholinesterase. Possible new roles for these endocannabinoids?

Biochimie

Volumn 93, Issue 9, 2011, Pages 1584-1591

  Romani, Rita ^a   Galeazzi, Roberta ^b   Rosi, Gabriella ^a   Fiorini, Rosamaria ^b   Pirisinu, Irene ^a   Ambrosini, Annarina ^b   Zolese, Giovanna ^b  

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Anandamide; Human plasma butyrylcholinesterase; Kinetic studies; Oleoylethanolamide; Palmitoylethanolamide

Indexed keywords

ANANDAMIDE; CHOLINESTERASE; N OLEOYLETHANOLAMINE; PALMIDROL;

ADULT; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOLECULAR DOCKING; PLASMA; X RAY CRYSTALLOGRAPHY;

ADULT; ARACHIDONIC ACIDS; BUTYRYLCHOLINESTERASE; CHOLINESTERASE INHIBITORS; CRYSTALLOGRAPHY, X-RAY; ENDOCANNABINOIDS; HUMANS; KINETICS; MALE; MIDDLE AGED; POLYUNSATURATED ALKAMIDES;

MAMMALIA;

EID: 79960841622     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.05.024     Document Type: Article

References (69)

1. J. Massoulié, L. Pezzementi, S. Bon, E. Krejci, and F.M. Vallette Molecular and cellular biology of cholinesterases Prog. Neurobiol. 41 1993 31 91 (Pubitemid 23140755)
2. P. Masson, and O. Lockridge Butyrylcholinesterase for protection from organophosphorus poisons: catalytic complexities and hysteretic behavior Arch. Biochem. Biophys. 494 2010 107 120
3. S. Darvesh, D.A. Hopkins, and C. Geula Neurobiology of butyrylcholinesterase Natl. Rev. Neurosci. 4 2003 131 138 (Pubitemid 37271383)
4. E. Giacobini Cholinesterases: new roles in brain function and in Alzheimer's disease Neurochem. Res. 28 2003 515 522 (Pubitemid 36314842)
5. R.S. Hoffman, R. Morasco, and L.R. Goldfrank Administration of purified human plasma cholinesterase protects against cocaine toxicity in mice J. Toxicol. Clin. Toxicol. 34 1996 259 266 (Pubitemid 26198099)
6. T.J. Lynch, C.E. Mattes, A. Singh, R.M. Bradley, R.O. Brady, and K.L. Dretchen Cocaine detoxification by human plasma butyrylcholinesterase Toxicol. Appl. Pharmacol. 145 1997 363 371 (Pubitemid 27346526)
7. G.N. Carmona, C.W. Schindler, M. Shoaib, R. Jufer, E.J. Cone, S.R. Goldberg, N.H. Greig, Q.S. Yu, and D.A. Gorelick Attenuation of cocaine-induced locomotor activity by butyrylcholinesterase Exp. Clin. Psychopharmacol. 6 1998 274 279 (Pubitemid 28393945)
8. E.G. Duysen, C.F. Bartels, and O. Lockridge Wild-type and A328W mutant human butyrylcholinesterase tetramers expressed in Chinese hamster ovary cells have a 16-hour half-life in the circulation and protect mice from cocaine toxicity J. Pharmacol. Exp. Ther. 302 2002 751 758 (Pubitemid 34787244)
9. H. Sun, M.L. Shen, Y.P. Pang, O. Lockridge, and S. Brimijoin Cocaine metabolism accelerated by a re-engineered human butyrylcholinesterase J. Pharmacol. Exp. Ther. 302 2002 710 716 (Pubitemid 34787239)
10. C.A. Broomfield, D.M. Maxwell, R.P. Solana, C.A. Castro, A.V. Finger, and D.E. Lenz Protection by butyrylcholinesterase against organophosphorus poisoning in nonhuman primates J. Pharmacol. Exp. Ther. 259 1991 633 638
11. R. Brandeis, L. Raveh, J. Grunwald, E. Cohen, and Y. Ashani Prevention of soman-induced cognitive deficits by pretreatment with human butyrylcholinesterase in rats Pharmacol. Biochem. Behav. 46 1993 889 896
12. L. Raveh, J. Grunwald, D. Marcus, Y. Papier, E. Cohen, and Y. Ashani Human butyrylcholinesterase as a general prophylactic antidote for nerve agent toxicity, In vitro and in vivo quantitative characterization Biochem. Pharmacol. 45 1993 2465 2474 (Pubitemid 23189540)
13. L. Raveh, E. Grauer, J. Grunwald, E. Cohen, and Y. Ashani The stoichiometry of protection against soman and VX toxicity in monkeys pretreated with human butyrylcholinesterase Toxicol. Appl. Pharmacol. 145 1997 43 53 (Pubitemid 27294768)
14. N. Allon, L. Raveh, E. Gilat, E. Cohen, J. Grunwald, and Y. Ashani Prophylaxis against soman inhalation toxicity in guinea pigs by pretreatment alone with human serum butyrylcholinesterase Toxicol. Sci. 43 1998 121 128 (Pubitemid 28363385)
15. B. Li, M. Sedlacek, I. Manoharan, R. Boopathy, E.G. Duysen, P. Masson, and O. Lockridge Butyrylcholinesterase, paraoxonase, and albumin esterase, but not carboxylesterase, are present in human plasma Biochem. Pharmacol. 70 2005 1673 1684 (Pubitemid 41540360)
16. D.M. Lambert, and C.J. Fowler The endocannabinoid system: drug targets, lead compounds, and potential therapeutic applications J. Med. Chem. 48 2005 5059 5087 (Pubitemid 41113892)
17. M. Bifulco, A.M. Malfitano, S. Pisanti, and C. Laezza Endocannabinoids in endocrine and related tumors Endocr. Relat. Cancer 15 2008 391 408
18. S.E. Lewis, and M. Maccarrone Endocannabinoids, sperm biology and human fertility Pharmacol. Res. 60 2009 126 131
19. K.D. Chapman Emerging physiological roles for Nacylphosphatidylethanolamine metabolism in plants: signal transduction and membrane protection Chem. Phys. Lipids 108 2000 221 230
20. T. Bisogno, M. Ventriglia, A. Milone, M. Mosca, G. Cimino, and V. Di Marzo Occurrence and metabolism of anandamide and related acyl-ethanolamides in ovaries of the sea urchin Paracentrotus lividus Biochim. Biophys. Acta 1345 1997 338 348 (Pubitemid 27171210)
21. N. Stella, and D. Piomelli Receptor-dependent formation of endogenous cannabinoids in cortical neurons Eur. J. Pharmacol. 425 2001 189 196 (Pubitemid 32770066)
22. I. Kaufmann, D. Hauer, V. Huge, M. Vogeser, P. Campolongo, A. Chouker, M. Thiel, and G. Schelling Enhanced anandamide plasma levels in patients with complex regional pain syndrome following traumatic injury: a preliminary report Eur. Surg. Res. 43 2009 325 329
23. B.B. Gorzalka, M.N. Hill, and C.J. Hillard Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders Neurosci. Biobehav. Rev. 32 2008 1152 1160
24. D. Schreiber, S. Harlfinger, B.M. Nolden, C.W. Gerth, U. Jaehde, E. Schömig, J. Klosterkötter, A. Giuffrida, G. Astarita, D. Piomelli, and F.M. Leweke Determination of anandamide and other fatty acyl ethanolamides in human serum by electrospray tandem mass spectrometry Anal. Biochem. 361 2007 162 168 (Pubitemid 46135393)
25. H. Schuel, J. Lani, L.J. Burkman, J. Lippes, K. Crickard, E. Forester, D. Piomelli, and A. Giuffrida N-Acylethanolamines in human reproductive fluids Chem. Phys. Lipids 121 2002 211 227 (Pubitemid 36044553)
26. E.V. Berdyshev, P.C. Schmid, R.J. Krebsbach, C.J. Hillard, C. Huang, N. Chen, Z. Dong, and H.H.O. Schmid Cannabinoid-receptor-independent cell signalling by N-acylethanolamines Biochem. J. 360 2001 67 75 (Pubitemid 33081950)
27. P.C. Schmid, R.J. Krebsbach, S.R. Perry, T.M. Dettmer, J.L. Maasson, and H.H.O. Schmid Occurrence and post-mortem generation of anandamide and other N-acylethanolamines in mammalian brain FEBS Lett. 375 1995 117 120
28. M. Maccarrone, M. Attin, M. Bari, A. Cartoni, C. Ledent, and A. Finazzi-Agr Anandamide degradation and N-acylethanolamines level in wild-type and CB1 cannabinoid receptor knockout mice of different ages J. Neurochem. 78 2001 339 348 (Pubitemid 32664415)
29. M.D. Randall Endocannabinoids and the haematological system Br. J. Pharmacol. 152 2007 671 675 (Pubitemid 350034975)
30. A. Ozalp, and B. Barroso Simultaneous quantitative analysis of N-acylethanolamides in clinical samples Anal. Biochem. 395 2009 68 76
31. C. Ahn, D.S. Johnson, and B.F. Cravatt Fatty acid amide hydrolase as a potential therapeutic target for the treatment of pain and CNS disorders Expert. Opin. Drug Discov. 7 2009 763 784
32. J.E. Casida, and G.B. Quistad Serine hydrolases targets of organophosphorus toxicants Chem. Biol. Interact. 157-158 2005 277 283 (Pubitemid 41757663)
33. A. Ambrosini, E. Bertoli, P. Mariani, F. Tanfani, M. Wozniak, and G. Zolese N-acylethanolamines as membrane topological stress compromising agents Biochim. Biophys. Acta 1148 1993 351 355 (Pubitemid 23173694)
34. J.S. Ralston, A.R. Main, B.F. Kilpatrick, and A.L. Chasson Use of procainamide gels in the purification of human and horse serum cholinesterases Biochem. J. 211 1983 243 250 (Pubitemid 13104397)
35. G.L. Ellman, D.K. Courtney, V. Andres, and R.M. Featherstone A new and rapid colorimetric determination of acetylcholinesterase activity Biochem. Pharmacol. 7 1961 88 95
36. D. Piomelli, M. Beltramo, S. Glasnapp, S.Y. Lin, A. Goutopoulos, X.Q. Xie, and A. Makriyannis Structural determinants for recognition and translocation by the anandamide transporter Proc. Natl. Acad. Sci. U.S.A. 96 1999 5802 5807 (Pubitemid 29234699)
37. P.H. Reggio, and H. Traore Conformational requirements for endocannabinoid interaction with the cannabinoid receptors, the anandamide transporter and fatty acid amidohydrolase Chem. Phys. Lipids 108 2000 15 35
38. A.D. MacKerell Jr., D. Bashford, M. Bellott, R.L. Dunbrack Jr., J.D. Evanseck, M.J. Field, S. Fisher, J. Gao, H. Guo, S. Ha, D.J. McCarthy, L. Kuchnir, K. Kuczera, F.T.K. Lau, C. Mattos, S. Michnick, T. Ngo, D.T. Nguyen, B. Prodhom, W.E. Reiher III, B. Roux, M. Schlenkrich, J.C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. 102 1998 3586 3616 (Pubitemid 128576688)
39. InsightII, Version Molecular Modeling System, User Guide 2000 Accelrys San Diego, CA
40. S. Darvesh, R.S. McDonald, A. Penwell, S. Conrad, K.V. Darvesh, D. Mataija, G. Gomez, A. Caines, R. Walsh, and E. Martin Structure-activity relationships for inhibition of human cholinesterases by alkyl amide phenothiazine derivatives Biorg. Med. Chem. 13 2005 211 222 (Pubitemid 39575706)
41. E. Murillo-Rodriguez, F. Désarnaud, and O. Prospéro- García Diurnal variation of arachidonoylethanolamine, palmitoylethanolamide and oleoylethanolamide in the brain of the rat Life Sci. 79 2006 30 37
42. C. Melchiorre, V. Andrisano, M.L. Bolognesi, R. Budriesi, A. Cavalli, V. Cavrini, M. Rosini, V. Tumiatti, and M. Recanatini Acetylcholinesterase noncovalent inhibitors based on a polyamine backbone for potential use against Alzheimer's disease J. Med. Chem. 41 1998 4186 4189 (Pubitemid 28498739)
43. A. Rampa, A. Bisi, P. Valenti, M. Recanatini, A. Cavalli, V. Andrisano, V. Cavrini, L. Fin, A. Buriani, and P. Giusti Acetylcholinesterase inhibitors: synthesis and structure-activity relationships of ω-[N-Methyl-N-(3- alkylcarbamoyloxyphenyl)- methyl] aminoalkoxy heteroaryl derivatives J. Med. Chem. 41 1998 3976 3986 (Pubitemid 28483475)
44. M.C. Fossi, C. Leonzio, A. Massi, L. Lari, and S. Casini Serum esterase inhibition in birds: a nondestructive biomarker to assess organophosphorus and carbamate contamination Arch. Environ. Contam. Toxicol. 23 1992 99 104
45. S.P. Browne, E.A. Slaughter, R.A. Couch, E.M. Rudnic, and A.M. McLean The influence of plasma butyrylcholinesterase concentration on the in vitro hydrolysis of cocaine in human plasma Biopharm. Drug Dispos. 19 1998 309 314 (Pubitemid 28313930)
46. A. Giuffrida, F. Rodriguez de Fonseca, F. Nava, P. Loubet- Lescoulié, and D. Pomelli Elevated circulating levels of anandamide after administration of the transport inhibitor, AM404 Eur. J. Pharmacol. 408 2000 161 168
47. G. Zolese, G. Falcioni, E. Bertoli, R. Galeazzi, M. Wozniak, Z. Wypych, E. Gratton, and A. Ambrosini Steady-state and time resolved fluorescence of albumins interacting with N-oleylethanolamine, a component of the endogenous N-acylethanolamines Proteins 40 2000 39 48 (Pubitemid 30368580)
48. I.N. Bojesen, and H.S. Hansen Binding of anandamide to bovine serum albumin J. Lipid Res. 44 2003 1790 1794 (Pubitemid 37185891)
49. G. Zolese, T. Bacchetti, A. Ambrosini, M. Wozniak, E. Bertoli, and G. Ferretti Increased plasma concentrations of Palmitoylethanolamide, an endogenous fatty acid amide, affect oxidative damage of human low-density lipoproteins: an in vitro study Atherosclerosis 182 2005 47 55 (Pubitemid 41188369)
50. A. Saxena, A.M.G. Redman, X. Jiang, O. Lockridge, and B.P. Doctor Differences in active site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase Biochemistry 36 1997 14642 14651 (Pubitemid 27524384)
51. P. Masson, P. Legrand, C.F. Bartels, M.T. Froment, L.M. Schopfer, and O. Lockridge Role of aspartate 70 and tryptophan 82 in binding of succinyldithiocholine to human butyrylcholinesterase Biochemistry 36 1997 2266 2277 (Pubitemid 27104721)
52. F. Nachon, L. Ehret-Sabatier, D. Loew, C. Colas, A. van Dorsselaer, and M. Goeldner Trp82 and Tyr332 are involved in two quaternary ammonium binding domains of human butyrylcholinesterase as revealed by photoaffinity labeling with [3H]DDF Biochemistry 37 1998 10507 10513 (Pubitemid 28357575)
53. A. Saxena, J.M. Fedorko, C.R. Vinayaka, R. Medhekar, Z. Radić, P. Taylor, O. Lockridge, and B.P. Doctor Aromatic amino-acid residues at the active and peripheral anionic sites control the binding of E2020 (Aricept) to cholinesterases Eur. J. Biochem. 270 2003 4447 4458 (Pubitemid 37452521)
54. P. Masson, W. Xie, M.T. Froment, V. Levitsky, P.L. Fortier, C. Albaret, and O. Lockridge Interaction between the peripheral site residues of human butyrylcholinesterase, D70 and Y332, in binding and hydrolysis of substrates Biochim. Biophys. Acta 1433 1999 281 293 (Pubitemid 29369063)
55. E. Bodur Human serum butyrylcholinesterase interactions with cisplatin and cyclophosphamide Biochimie 92 2010 979 984
56. I. Matias, M.P. Gonthier, S. Petrosino, L. Docimo, R. Capasso, L. Hoareau, P. Monteleone, R. Roche, A.A. Izzo, and V. Di Marzo Role and regulation of acylethanolamides in energy balance: focus on adipocytes and β-cells Br. J. Pharmacol. 152 2007 676 690 (Pubitemid 350041540)
57. L. Jean-Gilles, S. Feng, C.R. Tench, V. Chapman, D.A. Kendall, D.A. Barrett, and C.S. Constantinescu Plasma endocannabinoid levels in multiple sclerosis J. Neurol. Sci. 287 2009 212 215
58. F. Oveisi, S. Gaetani, K. Tai-Pang Eng, and D. Piomelli Oleoylethanolamide inhibits food intake in free-feeding rats after oral administration Pharmacol. Res. 49 2004 461 466 (Pubitemid 38283867)
59. B. Zencirci Pseudocholinesterase enzyme deficiency: a case series and review of the literature Cases J. 2 2009 9148 9152
60. D.A. Grelick, E.L. Gardner, and Z.X. Xi Agents in development for the management of cocaine abuse Drugs 64 2004 1547 1573 (Pubitemid 38981839)
61. F. Zheng, and C.G. Zhan Structure-and-mechanism-based design and discovery of therapeutics for cocaine overdose and addiction Org. Biomol. Chem. 6 2008 836 843 (Pubitemid 351653352)
62. F. Zheng, and C.G. Zhan Recent progress in protein drug design and discovery with a focus on novel approaches to the development of anticocaine medications Future Med. Chem. 1 2009 515 528
63. A. Saxena, C. Luo, and B.P. Doctor Developing procedures for the large-scale purification of human serum Butyrylcholinesterase Protein Exp. Purif. 61 2008 191 196
64. P.M.W. Lam, T.H. Marczylo, and J.C. Konje Simultaneous measurement of three N-acylethanolamides in human bio-matrices using ultra performance liquid chromatography-tandem mass spectrometry Anal. Bioanal. Chem. 398 2010 2089 2097
65. R. Jumpertz, A. Guijarro, R.E. Pratley, D. Piomelli, and J. Krakoff Central and peripheral endocannabinoids and cognate acylethanolamides in humans: association with race, adiposity, and energy expenditure J. Clin. Endocrinol. Metab. 96 2011 787 791
66. M.M. Mesulam, A. Guillozet, P. Shaw, A. Levey, E.G. Duysen, and O. Lockridge Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine Neuroscience 110 2002 627 639 (Pubitemid 34270534)
67. N.H. Greig, T. Utsuki, D.K. Ingram, Y. Wang, G. Pepeu, C. Scali, Q.S. Yu, J. Mamczarz, H.W. Holloway, T. Giordano, D. Chen, K. Furukawa, K. Sambamurti, A. Brossi, and D.K. Lahiri Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent Proc. Natl. Acad. Sci. U.S.A. 102 2005 17213 17218 (Pubitemid 41692709)
68. T. Darreh-Shori, O. Almkvist, Z.Z. Guan, A. Garlind, B. Strandberg, A.L. Svensson, H. Soreq, E. Hellström-Lindahl, and A. Nordberg Sustained cholinesterase inhibition in AD patients receiving rivastigmine for 12 months Neurology 59 2002 563 572 (Pubitemid 34919991)
69. Q.S. Yu, H.W. Holloway, T. Utsuki, A. Brossi, and N.H. Greig Phenserine-based synthesis of novel selective inhibitors of butyrylcholinesterase for Alzheimer's disease J. Med. Chem. 42 1999 1855 1861 (Pubitemid 29244980)