A catalytically silent FAAH-1 variant drives anandamide transport in neurons

Nature Neuroscience

Volumn 15, Issue 1, 2012, Pages 64-69

  Fu, Jin ^a   Bottegoni, Giovanni ^b   Sasso, Oscar ^b   Bertorelli, Rosalia ^b   Rocchia, Walter ^b   Masetti, Matteo ^b   Guijarro, Ana ^a   Lodola, Alessio ^c   Armirotti, Andrea ^b   Garau, Gianpiero ^b   Bandiera, Tiziano ^b   Reggiani, Angelo ^b   Mor, Marco ^c   Cavalli, Andrea ^b,d   Piomelli, Daniele ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANANDAMIDE; ARN 272; FATTY ACID AMIDASE; FATTY ACID AMIDASE INHIBITOR; FATTY ACID AMIDE HYDROLASE 1 LIKE ANANDAMIDE TRANSPORTER; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; OMDM 1; PHTHALAZINE DERIVATIVE; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EDEMA; ENZYME ACTIVITY; HYPERALGESIA; MALE; MOUSE; NERVE CELL; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BENZYL COMPOUNDS; NEURONS; POLYUNSATURATED ALKAMIDES; PROTEIN TRANSPORT; RATS;

EID: 84555198880     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2986     Document Type: Article

References (49)

1. Piomelli, D., Astarita, G. & Rapaka, R. A neuroscientist's guide to lipidomics. Nat. Rev. Neurosci. 8, 743-754 (2007). (Pubitemid 47462119)
2. Devane, W.A. et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949 (1992). (Pubitemid 23026736)
3. Beltramo, M. et al. Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277, 1094-1097 (1997). (Pubitemid 27371630)
4. 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, 631-638 (1997). (Pubitemid 27327964)
5. Hillard, C.J., Shi, L., Tuniki, V.R., Falck, J.R. & Campbell, W.B. Studies of anandamide accumulation inhibitors in cerebellar granule neurons: comparison to inhibition of fatty acid amide hydrolase. J. Mol. Neurosci. 33, 18-24 (2007). (Pubitemid 47574953)
6. Cravatt, B.F. et al. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA 98, 9371-9376 (2001). (Pubitemid 32743923)
7. McKinney, M.K. & Cravatt, B.F. Structure and function of fatty acid amide hydrolase. Annu. Rev. Biochem. 74, 411-432 (2005). (Pubitemid 40995513)
8. Wei, B.Q., Mikkelsen, T.S., McKinney, M.K., Lander, E.S. & Cravatt, B.F. A second fatty acid amide hydrolase with variable distribution among placental mammals. J. Biol. Chem. 281, 36569-36578 (2006). (Pubitemid 46049797)
9. Hillard, C.J. & Jarrahian, A. Cellular accumulation of anandamide: consensus and controversy. Br. J. Pharmacol. 140, 802-808 (2003). (Pubitemid 37464061)
10. Di Marzo, V. Targeting the endocannabinoid system: to enhance or reduce? Nat. Rev. Drug Discov. 7, 438-455 (2008). (Pubitemid 351649182)
11. Piomelli, D. et al. Structural determinants for recognition and translocation by the anandamide transporter. Proc. Natl. Acad. Sci. USA 96, 5802-5807 (1999). (Pubitemid 29234699)
12. Glaser, S.T. et al. Evidence against the presence of an anandamide transporter. Proc. Natl. Acad. Sci. USA 100, 4269-4274 (2003). (Pubitemid 36418192)
13. Jacobsson, S.O. & 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, 1743-1754 (2001). (Pubitemid 32397966)
14. Matlin, A.J., Clark, F. & Smith, C.W. Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol. 6, 386-398 (2005). (Pubitemid 40637856)
15. Bracey, M.H., Hanson, M.A., Masuda, K.R., Stevens, R.C. & Cravatt, B.F. Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling. Science 298, 1793-1796 (2002). (Pubitemid 35404124)
16. Patricelli, M.P. & Cravatt, B.F. Fatty acid amide hydrolase competitively degrades bioactive amides and esters through a nonconventional catalytic mechanism. Biochemistry 38, 14125-14130 (1999).
17. 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, 1473-1481 (2003). (Pubitemid 36559598)
18. Alexander, J.P. & Cravatt, B.F. Mechanism of carbamate inactivation of FAAH: implications for the design of covalent inhibitors and in vivo functional probes for enzymes. Chem. Biol. 12, 1179-1187 (2005). (Pubitemid 41628253)
19. Speers, A.E. & Wu, C.C. Proteomics of integral membrane proteins-theory and application. Chem. Rev. 107, 3687-3714 (2007). (Pubitemid 47322748)
20. Ortega-Gutiérrez, S., Hawkins, E.G., Viso, A., Lopez-Rodriguez, M.L. & Cravatt, B.F. 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 (2004). (Pubitemid 38808274)
21. Kathuria, S. et al. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81 (2003). (Pubitemid 36098263)
22. Yates, M.L. & Barker, E.L. Inactivation and biotransformation of the endogenous cannabinoids anandamide and 2-arachidonoylglycerol. Mol. Pharmacol. 76, 11-17 (2009).
23. Ligresti, A. et al. Further evidence for the existence of a specific process for the membrane transport of anandamide. Biochem. J. 380, 265-272 (2004). (Pubitemid 38725751)
24. La Rana, G. et al. 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 (2006). (Pubitemid 43764143)
25. Maione, S. et al. Antinociceptive effects of tetrazole inhibitors of endocannabinoid inactivation: cannabinoid and non-cannabinoid receptor-mediated mechanisms. Br. J. Pharmacol. 155, 775-782 (2008).
26. Lichtman, A.H. et al. Reversible inhibitors of fatty acid amide hydrolase that promote analgesia: evidence for an unprecedented combination of potency and selectivity. J. Pharmacol. Exp. Ther. 311, 441-448 (2004). (Pubitemid 39391527)
27. Russo, R. et al. The fatty acid amide hydrolase inhibitor URB597 (cyclohexylcarbamic acid 3′-carbamoylbiphenyl-3-yl ester) reduces neuropathic pain after oral administration in mice. J. Pharmacol. Exp. Ther. 322, 236-242 (2007). (Pubitemid 46956375)
28. Beltramo, M. & Piomelli, D. Carrier-mediated transport and enzymatic hydrolysis of the endogenous cannabinoid 2-arachidonylglycerol. Neuroreport 11, 1231-1235 (2000). (Pubitemid 30262964)
29. Bisogno, T. et al. The uptake by cells of 2-arachidonoylglycerol, an endogenous agonist of cannabinoid receptors. Eur. J. Biochem. 268, 1982-1989 (2001). (Pubitemid 32852939)
30. Niot, I., Poirier, H., Tran, T.T. & Besnard, P. Intestinal absorption of long-chain fatty acids: evidence and uncertainties. Prog. Lipid Res. 48, 101-115 (2009).
31. Kanai, N. et al. Identification and characterization of a prostaglandin transporter. Science 268, 866-869 (1995).
32. Reese-Wagoner, A., Thompson, J. & Banaszak, L. Structural properties of the adipocyte lipid binding protein. Biochim. Biophys. Acta 1441, 106-116 (1999). (Pubitemid 29537731)
33. Schwartz, G.J. et al. The lipid messenger OEA links dietary fat intake to satiety. Cell Metab. 8, 281-288 (2008).
34. Gulyas, A.I. et al. Segregation of two endocannabinoid-hydrolyzing enzymes into pre-and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur. J. Neurosci. 20, 441-458 (2004). (Pubitemid 38969629)
35. Bojesen, I.N. & Hansen, H.S. Binding of anandamide to bovine serum albumin. J. Lipid Res. 44, 1790-1794 (2003). (Pubitemid 37185891)
36. Kaczocha, M., Glaser, S.T. & Deutsch, D.G. Identification of intracellular carriers for the endocannabinoid anandamide. Proc. Natl. Acad. Sci. USA 106, 6375-6380 (2009).
37. Maccarrone, M., Dainese, E. & Oddi, S. Intracellular trafficking of anandamide: new concepts for signaling. Trends Biochem. Sci. 35, 601-608 (2010).
38. Oddi, S. et al. Molecular identification of albumin and Hsp70 as cytosolic anandamide-binding proteins. Chem. Biol. 16, 624-632 (2009).
39. Rosso, L. & Gould, I.R. Structure and dynamics of phospholipid bilayers using recently developed general all-atom force fields. J. Comput. Chem. 29, 24-37 (2008).
40. Abagyan, R. & Totrov, M. Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J. Mol. Biol. 235, 983-1002 (1994). (Pubitemid 24047836)
41. Phillips, J.C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005). (Pubitemid 43078511)
42. Hornak, V. et al. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725 (2006). (Pubitemid 44583220)
43. Rocchia, W., Alexov, E. & Honig, B. Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions. J. Phys. Chem. B 105, 6507-6514 (2001); addition/correction 105, 6754 (2001). (Pubitemid 35339019)
44. Seierstad, M. & Breitenbucher, J.G. Discovery and development of fatty acid amide hydrolase (FAAH) inhibitors. J. Med. Chem. 51, 7327-7343 (2008).
45. Evans, M.S., Collings, M.A. & Brewer, G.J. Electrophysiology of embryonic, adult and aged rat hippocampal neurons in serum-free culture. J. Neurosci. Methods 79, 37-46 (1998). (Pubitemid 28248239)
46. Pearson, G.D. & Mekalanos, J.J. Molecular cloning of Vibrio cholerae enterotoxin genes in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 79, 2976-2980 (1982). (Pubitemid 12058599)
47. Fu, J. et al. Food intake regulates oleoylethanolamide formation and degradation in the proximal small intestine. J. Biol. Chem. 282, 1518-1528 (2007). (Pubitemid 47076553)
48. Li, X. et al. Expression genetics identifies spinal mechanisms supporting formalin late phase behaviors. Mol. Pain 6, 11 (2010).
49. Hargreaves, K., Dubner, R., Brown, F., Flores, C. & Joris, J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32, 77-88 (1988).