Endocannabinoid functions controlling neuronal specification during brain development

Molecular and Cellular Endocrinology

Volumn 286, Issue 1-2 SUPPL. 1, 2008, Pages

  Harkany, Tibor ^a,b   Keimpema, Erik ^a   Barabás, Klaudia ^a   Mulder, Jan ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Brain development; Embryo; Interneuron; Lineage; Pyramidal cell; Synapse

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABIS; ENDOCANNABINOID;

ARTICLE; BRAIN DEVELOPMENT; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; ENDOCYTOSIS; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; SYNAPTOGENESIS; TELENCEPHALON;

ANIMALS; BODY PATTERNING; BRAIN; ENDOCANNABINOIDS; HUMANS; NEURONS; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION;

EID: 42249098694     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.02.011     Document Type: Article

References (104)

1. Abe H., Yanagawa Y., Kanbara K., Maemura K., Hayasaki H., Azuma H., Obata K., Katsuoka Y., Yabumoto M., and Watanabe M. Epithelial localization of green fluorescent protein-positive cells in epididymis of the GAD67-GFP knock-in mouse. J. Androl. 26 (2005) 568-577
2. Aguado T., Monory K., Palazuelos J., Stella N., Cravatt B., Lutz B., Marsicano G., Kokaia Z., Guzman M., and Galve-Roperh I. The endocannabinoid system drives neural progenitor proliferation. FASEB J. 19 (2005) 1704-1706
3. Aguado T., Palazuelos J., Monory K., Stella N., Cravatt B., Lutz B., Marsicano G., Kokaia Z., Guzman M., and Galve-Roperh I. The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J. Neurosci. 26 (2006) 1551-1561
4. Arevalo-Martin A., Garcia-Ovejero D., Rubio-Araiz A., Gomez O., Molina-Holgado F., and Molina-Holgado E. Cannabinoids modulate Olig2 and polysialylated neural cell adhesion molecule expression in the subventricular zone of post-natal rats through cannabinoid receptor 1 and cannabinoid receptor 2. Eur. J. Neurosci. 26 (2007) 1548-1559
5. Baker D., Pryce G., Davies W.L., and Hiley C.R. In silico patent searching reveals a new cannabinoid receptor. Trends Pharmacol. Sci. 27 (2006) 1-4
6. Berghuis P., Dobszay M.B., Ibanez R.M., Ernfors P., and Harkany T. Turning the heterogeneous into homogeneous: studies on selectively isolated GABAergic interneuron subsets. Int. J. Dev. Neurosci. 22 (2004) 533-543
7. Berghuis P., Dobszay M.B., Wang X., Spano S., Ledda F., Sousa K.M., Schulte G., Ernfors P., Mackie K., Paratcha G., Hurd Y.L., and Harkany T. Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 19115-19120
8. Berghuis P., Rajnicek A.M., Morozov Y.M., Ross R.A., Mulder J., Urban G.M., Monory K., Marsicano G., Matteoli M., Canty A., Irving A.J., Katona I., Yanagawa Y., Rakic P., Lutz B., Mackie K., and Harkany T. Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316 (2007) 1212-1216
9. Bernard C., Milh M., Morozov Y.M., Ben Ari Y., Freund T.F., and Gozlan H. Altering cannabinoid signaling during development disrupts neuronal activity. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 9388-9393
10. Berrendero F., Sepe N., Ramos J.A., Di M., and Fernandez-Ruiz V.J.J. Analysis of cannabinoid receptor binding and mRNA expression and endogenous cannabinoid contents in the developing rat brain during late gestation and early postnatal period. Synapse 33 (1999) 181-191
11. Bisogno T., Howell F., Williams G., Minassi A., Cascio M.G., Ligresti A., Matias I., Schiano-Moriello A., Paul P., Williams E.J., Gangadharan U., Hobbs C., Di M., and Doherty V.P. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163 (2003) 463-468
12. Brown A.J. Novel cannabinoid receptors. Br. J. Pharmacol. 152 (2007) 567-575
13. Coutts A.A., Anavi-Goffer S., Ross R.A., MacEwan D.J., Mackie K., Pertwee R.G., and Irving A.J. Agonist-induced internalization and trafficking of cannabinoid CB1 receptors in hippocampal neurons. J. Neurosci. 21 (2001) 2425-2433
14. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., and Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384 (1996) 83-87
15. D'Antona A.M., Ahn K.H., and Kendall D.A. Mutations of CB1 T210 produce active and inactive receptor forms: correlations with ligand affinity, receptor stability, and cellular localization. Biochemistry 45 (2006) 5606-5617
16. Daigle T.L., Kearn C.S., and Mackie K. Rapid CB(1) cannabinoid receptor desensitization defines the time course of ERK1/2 MAP kinase signaling. Neuropharmacology 54 (2008) 36-44
17. Derkinderen P., Toutant M., Burgaya F., Le Bert M., Siciliano J.C., de F., Gelman V., and Girault M.J.A. Regulation of a neuronal form of focal adhesion kinase by anandamide. Science 273 (1996) 1719-1722
18. Derkinderen P., Valjent E., Toutant M., Corvol J.C., Enslen H., Ledent C., Trzaskos J., Caboche J., and Girault J.A. Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J. Neurosci. 23 (2003) 2371-2382
19. Devi L.A. G-protein-coupled receptor dimers in the lime light. Trends Pharmacol. Sci. 21 (2000) 324-326
20. Dinh T.P., Carpenter D., Leslie F.M., Freund T.F., Katona I., Sensi S.L., Kathuria S., and Piomelli D. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 10819-10824
21. Egertova M., Simon G.M., Cravatt B.F., and Elphick M.R. Localization of N-acyl phosphatidylethanolamine phospholipase D (NAPE-PLD) expression in mouse brain: a new perspective on N-acylethanolamines as neural signaling molecules. J. Comp Neurol. 506 (2007) 604-615
22. Ellis J., Pediani J.D., Canals M., Milasta S., and Milligan G. Orexin-1 receptor-cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and -independent coordinated alterations of receptor localization and function. J. Biol. Chem. 281 (2006) 38812-38824
23. Fernandez-Ruiz J., Berrendero F., Hernandez M.L., and Ramos J.A. The endogenous cannabinoid system and brain development. Trends Neurosci. 23 (2000) 14-20
24. Galve-Roperh I., Aguado T., Palazuelos J., and Guzman M. The endocannabinoid system and neurogenesis in health and disease. Neuroscientist 13 (2007) 109-114
25. Galve-Roperh I., Aguado T., Rueda D., Velasco G., and Guzman M. Endocannabinoids: a new family of lipid mediators involved in the regulation of neural cell development. Curr. Pharm. Des. 12 (2006) 2319-2325
26. Galve-Roperh I., Sanchez C., Cortes M.L., del Pulgar T.G., Izquierdo M., and Guzman M. Anti-tumoral action of cannabinoids: involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat. Med. 6 (2000) 313-319
27. Ghosh S., Preet A., Groopman J.E., and Ganju R.K. Cannabinoid receptor CB2 modulates the CXCL12/CXCR4-mediated chemotaxis of T lymphocytes. Mol. Immunol. 43 (2006) 2169-2179
28. Guzman M. Cannabinoids: potential anticancer agents. Nat. Rev. Cancer 3 (2003) 745-755
29. Guzman M., Sanchez C., and Galve-Roperh I. Control of the cell survival/death decision by cannabinoids. J. Mol. Med. 78 (2001) 613-625
30. Guzman M., Sanchez C., and Galve-Roperh I. Cannabinoids and cell fate. Pharmacol. Ther. 95 (2002) 175-184
31. Harkany T., Guzman M., Galve-Roperh I., Berghuis P., Devi L.A., and Mackie K. The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol. Sci. 28 (2007) 83-92
32. (o/i)-coupled cannabinoid receptor-mediated neurite outgrowth involves Rap regulation of Src and Stat3. J. Biol. Chem. 280 (2005) 33426-33434
33. Hsieh C., Brown S., Derleth C., and Mackie K. Internalization and recycling of the CB1 cannabinoid receptor. J. Neurochem. 73 (1999) 493-501
34. Huizink A.C., and Mulder E.J. Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neurosci. Biobehav. Rev. 30 (2006) 24-41
35. Iyengar R. Teaching resources. Introduction: overview of pathways and networks and GPCR signaling. Sci. STKE 2005 (2005) tr4
36. Jin K., Xie L., Kim S.H., Parmentier-Batteur S., Sun Y., Mao X.O., Childs J., and Greenberg D.A. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol. Pharmacol. 66 (2004) 204-208
37. Johns D.G., Behm D.J., Walker D.J., Ao Z., Shapland E.M., Daniels D.A., Riddick M., Dowell S., Staton P.C., Green P., Shabon U., Bao W., Aiyar N., Yue T.L., Brown A.J., Morrison A.D., and Douglas S.A. The novel endocannabinoid receptor GPR55 is activated by atypical cannabinoids but does not mediate their vasodilator effects. Br. J. Pharmacol. 152 (2007) 825-831
38. o/i-triggered proteasomal degradation of Rap1GAPII. J. Biol. Chem. 280 (2005) 11413-11421
39. Katona I., Urban G.M., Wallace M., Ledent C., Jung K.M., Piomelli D., Mackie K., and Freund T.F. Molecular composition of the endocannabinoid system at glutamatergic synapses. J. Neurosci. 26 (2006) 5628-5637
40. Kreitzer A.C., and Regehr W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29 (2001) 717-727
41. Kurihara R., Tohyama Y., Matsusaka S., Naruse H., Kinoshita E., Tsujioka T., Katsumata Y., and Yamamura H. Effects of peripheral cannabinoid receptor ligands on motility and polarization in neutrophil-like HL60 cells and human neutrophils. J. Biol. Chem. 281 (2006) 12908-12918
42. Lauckner J.E., Hille B., and Mackie K. The cannabinoid agonist WIN55.212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 19144-19149
43. Lauckner J.E., Jensen J.B., Chen H.Y., Lu H.C., Hille B., and Mackie K. GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc. Natl. Acad. Sci. U.S.A. (2008)
44. Leterrier C., Bonnard D., Carrel D., Rossier J., and Lenkei Z. Constitutive endocytic cycle of the CB1 cannabinoid receptor. J. Biol. Chem. 279 (2004) 36013-36021
45. Leterrier C., Laine J., Darmon M., Boudin H., Rossier J., and Lenkei Z. Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J. Neurosci. 26 (2006) 3141-3153
46. Liu J., Wang L., Harvey-White J., Osei-Hyiaman D., Razdan R., Gong Q., Chan A.C., Zhou Z., Huang B.X., Kim H.Y., and Kunos G. A biosynthetic pathway for anandamide. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13345-13350
47. Lutz B. On-demand activation of the endocannabinoid system in the control of neuronal excitability and epileptiform seizures. Biochem. Pharmacol. 68 (2004) 1691-1698
48. Maccarrone M., Rossi S., Bari M., De C., Fezza V., Musella F., Gasperi A., Prosperetti V., Bernardi C., Finazzi-Agro G., Cravatt A., and Centonze B.F.D. Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat. Neurosci. 11 (2008) 152-159
49. Mackie K., and Stella N. Cannabinoid receptors and endocannabinoids: evidence for new players. AAPS J. 8 (2006) E298-E306
50. Maione S., Bisogno T., de N., Palazzo V., Cristino E., Valenti L., Petrosino M., Guglielmotti S., Rossi V., and Di F.M.V. Elevation of endocannabinoid levels in the ventrolateral periaqueductal grey through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. J. Pharmacol. Exp. Ther. 316 (2006) 969-982
51. Matias I., and Di Marzo V. Endocannabinoid synthesis and degradation, and their regulation in the framework of energy balance. J. Endocrinol. Invest. 29 (2006) 15-26
52. Mato S., Del Olmo E., and Pazos A. Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur. J. Neurosci. 17 (2003) 1747-1754
53. Matyas F., Urban G.M., Watanabe M., Mackie K., Zimmer A., Freund T.F., and Katona I. Identification of the sites of 2-arachidonoylglycerol synthesis and action imply retrograde endocannabinoid signaling at both GABAergic and glutamatergic synapses in the ventral tegmental area. Neuropharmacology 54 (2008) 95-107
54. McDonald N.A., Henstridge C.M., Connolly C.N., and Irving A.J. An essential role for constitutive endocytosis, but not activity, in the axonal targeting of the CB1 cannabinoid receptor. Mol. Pharmacol. 71 (2007) 976-984
55. McDonald N.A., Henstridge C.M., Connolly C.N., and Irving A.J. Generation and functional characterization of fluorescent N-terminally tagged CB(1) receptor chimeras for live-cell imaging. Mol. Cell Neurosci. 35 (2007) 237-248
56. McHugh D., Tanner C., Mechoulam R., Pertwee R.G., and Ross R.A. Inhibition of human neutrophil chemotaxis by endogenous cannabinoids and phytocannabinoids: evidence for a site distinct from CB1 and CB2. Mol. Pharmacol. (2007)
57. Mereu G., Fa M., Ferraro L., Cagiano R., Antonelli T., Tattoli M., Ghiglieri V., Tanganelli S., Gessa G.L., and Cuomo V. Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 4915-4920
58. Miller A.M., and Stella N. CB(2) receptor-mediated migration of immune cells: it can go either way. Br. J. Pharmacol. 153 (2007) 299-308
59. Molina-Holgado E., Vela J.M., Arevalo-Martin A., Almazan G., Molina-Holgado F., Borrell J., and Guaza C. Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J. Neurosci. 22 (2002) 9742-9753
60. Molina-Holgado F., Rubio-Araiz A., Garcia-Ovejero D., Williams R.J., Moore J.D., Arevalo-Martin A., Gomez-Torres O., and Molina-Holgado E. CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur. J. Neurosci. 25 (2007) 629-634
61. Morishita J., Okamoto Y., Tsuboi K., Ueno M., Sakamoto H., Maekawa N., and Ueda N. Regional distribution and age-dependent expression of N-acylphosphatidylethanolamine-hydrolyzing phospholipase D in rat brain. J. Neurochem. 94 (2005) 753-762
62. Morozov Y.M., Ben Ari Y., and Freund T.F. The spatial and temporal pattern of fatty acid amide hydrolase expression in rat hippocampus during postnatal development. Eur. J. Neurosci. 20 (2004) 459-466
63. Muccioli G.G., Xu C., Odah E., Cudaback E., Cisneros J.A., Lambert D.M., Lopez Rodriguez M.L., Bajjalieh S., and Stella N. Identification of a novel endocannabinoid-hydrolyzing enzyme expressed by microglial cells. J. Neurosci. 27 (2007) 2883-2889
64. Mulder A.M., and Cravatt B.F. Endocannabinoid metabolism in the absence of fatty acid amide hydrolase (FAAH): discovery of phosphorylcholine derivatives of N-acyl ethanolamines. Biochemistry 45 (2006) 11267-11277
65. Mulder, J., Aguado, T., Keimpema, E., Barabas, K., Ballester Rosado, C.J., Nguyen, L., Monory, K., Marsicano, G., Di Marzo, V., Hurd, Y.L., Guillemot, F., Mackie, K., Lutz, B., Guzman, M., Lu, H.C., Galve-Roperh, I. Harkany, T. submitted for publication. Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning.
66. Munro S., Thomas K.L., and Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365 (1993) 61-65
67. Niehaus J.L., Liu Y., Wallis K.T., Egertova M., Bhartur S.G., Mukhopadhyay S., Shi S., He H., Selley D.E., Howlett A.C., Elphick M.R., and Lewis D.L. CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Mol. Pharmacol. 72 (2007) 1557-1566
68. Ohno-Shosaku T., Tsubokawa H., Mizushima I., Yoneda N., Zimmer A., and Kano M. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J. Neurosci. 22 (2002) 3864-3872
69. Oka S., Nakajima K., Yamashita A., Kishimoto S., and Sugiura T. Identification of GPR55 as a lysophosphatidylinositol receptor. Biochem. Biophys. Res. Commun. 362 (2007) 928-934
70. Okamoto Y., Wang J., Morishita J., and Ueda N. Biosynthetic pathways of the endocannabinoid anandamide. Chem. Biodivers. 4 (2007) 1842-1857
71. Piomelli D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4 (2003) 873-884
72. Preet A., Ganju R.K., and Groopman J.E. Delta(9)-tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene (2007)
73. Rajesh M., Mukhopadhyay P., Hasko G., Huffman J.W., Mackie K., and Pacher P. CB(2) cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br. J. Pharmacol. 153 (2008) 347-357
74. Rimmerman N., Hughes H.V., Bradshaw H.B., Pazos M.X., Mackie K., Prieto A.L., and Walker J.M. Compartmentalization of endocannabinoids into lipid rafts in a dorsal root ganglion cell line. Br. J. Pharmacol. 153 (2008) 380-389
75. Rinaldi-Carmona M., Le Duigou A., Oustric D., Barth F., Bouaboula M., Carayon P., Casellas P., and Le Fur G. Modulation of CB1 cannabinoid receptor functions after a long-term exposure to agonist or inverse agonist in the Chinese hamster ovary cell expression system. J. Pharmacol. Exp. Ther. 287 (1998) 1038-1047
76. Rios C., Gomes I., and Devi L.A. Mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br. J. Pharmacol. 148 (2006) 387-395
77. Roche J.P., Bounds S., Brown S., and Mackie K. A mutation in the second transmembrane region of the CB1 receptor selectively disrupts G protein signaling and prevents receptor internalization. Mol. Pharmacol. 56 (1999) 611-618
78. Romero J., Garcia-Palomero E., Berrendero F., Garcia-Gil L., Hernandez M.L., Ramos J.A., and Fernandez-Ruiz J.J. Atypical location of cannabinoid receptors in white matter areas during rat brain development. Synapse 26 (1997) 317-323
79. Rueda D., Navarro B., Martinez-Serrano A., Guzman M., and Galve-Roperh I. The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J. Biol. Chem. 277 (2002) 46645-46650
80. Ryberg E., Larsson N., Sjogren S., Hjorth S., Hermansson N.O., Leonova J., Elebring T., Nilsson K., Drmota T., and Greasley P.J. The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol. 152 (2007) 1092-1101
81. Ryberg E., Vu H.K., Larsson N., Groblewski T., Hjorth S., Elebring T., Sjogren S., and Greasley P.J. Identification and characterisation of a novel splice variant of the human CB1 receptor. FEBS Lett. 579 (2005) 259-264
82. Sampo B., Kaech S., Kunz S., and Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37 (2003) 611-624
83. Sawzdargo M., Nguyen T., Lee D.K., Lynch K.R., Cheng R., Heng H.H., George S.R., and O'Dowd B.F. Identification and cloning of three novel human G protein-coupled receptor genes GPR52, PsiGPR53 and GPR55: GPR55 is extensively expressed in human brain. Brain Res. Mol. Brain Res. 64 (1999) 193-198
84. Seong E., Wainer B.H., Hughes E.D., Saunders T.L., Burmeister M., and Faundez V. Genetic analysis of the neuronal and ubiquitous AP-3 adaptor complexes reveals divergent functions in brain. Mol. Biol. Cell 16 (2005) 128-140
85. Simon, G.M., Cravatt, B.F., 2006. Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for {alpha}/beta-hydrolase 4 in this pathway. J. Biol. Chem. 281, 26465-26472.
86. Song Z.H., and Zhong M. CB1 cannabinoid receptor-mediated cell migration. J. Pharmacol. Exp. Ther. 294 (2000) 204-209
87. Stoddart L.A., Brown A.J., and Milligan G. Uncovering the pharmacology of the G protein-coupled receptor GPR40: high apparent constitutive activity in guanosine 5′-O-(3-[35S]thio)triphosphate binding studies reflects binding of an endogenous agonist. Mol. Pharmacol. 71 (2007) 994-1005
88. Turu G., Simon A., Gyombolai P., Szidonya L., Bagdy G., Lenkei Z., and Hunyady L. The role of diacylglycerol lipase in constitutive and angiotensin AT1 receptor-stimulated cannabinoid CB1 receptor activity. J. Biol. Chem. 282 (2007) 7753-7757
89. Uchigashima M., Narushima M., Fukaya M., Katona I., Kano M., and Watanabe M. Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 27 (2007) 3663-3676
90. Ueda N., Okamoto Y., and Morishita J. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D: a novel enzyme of the beta-lactamase fold family releasing anandamide and other N-acylethanolamines. Life Sci. 77 (2005) 1750-1758
91. Ujike H., Takaki M., Nakata K., Tanaka Y., Takeda T., Kodama M., Fujiwara Y., Sakai A., and Kuroda S. CNR1, central cannabinoid receptor gene, associated with susceptibility to hebephrenic schizophrenia. Mol. Psychiatry 7 (2002) 515-518
92. van der Stelt M., and Di Marzo V. Anandamide as an intracellular messenger regulating ion channel activity. Prostaglandins Other Lipid Mediat. 77 (2005) 111-122
93. Wager-Miller J., Westenbroek R., and Mackie K. Dimerization of G protein-coupled receptors: CB1 cannabinoid receptors as an example. Chem. Phys. Lipids 121 (2002) 83-89
94. Waldhoer M., Casarosa P., Rosenkilde M.M., Smit M.J., Leurs R., Whistler J.L., and Schwartz T.W. The carboxyl terminus of human cytomegalovirus-encoded 7 transmembrane receptor US28 camouflages agonism by mediating constitutive endocytosis. J. Biol. Chem. 278 (2003) 19473-19482
95. Walter L., Franklin A., Witting A., Wade C., Xie Y., Kunos G., Mackie K., and Stella N. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J. Neurosci. 23 (2003) 1398-1405
96. Wang X., Dow-Edwards D., Keller E., and Hurd Y.L. Preferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain. Neuroscience 118 (2003) 681-694
97. Watson, S., Chambers, D., Hobbs, C., Doherty, P., Graham, A., in press. The cannabinoid receptor, CB1, is required for normal axonal growth and fasciculation. Mol. Cell Neurosci.
98. Wei B.Q., Mikkelsen T.S., McKinney M.K., Lander E.S., and Cravatt B.F. A second fatty acid amide hydrolase with variable distribution among placental mammals. J. Biol. Chem. 281 (2006) 36569-36578
99. Weiser M., and Noy S. Interpreting the association between cannabis use and increased risk for schizophrenia. Dialogues Clin. Neurosci. 7 (2005) 81-85
100. Whistler J.L., Gerber B.O., Meng E.C., Baranski T.J., von Zastrow M., and Bourne H.R. Constitutive activation and endocytosis of the complement factor 5a receptor: evidence for multiple activated conformations of a G protein-coupled receptor. Traffic 3 (2002) 866-877
101. Williams E.J., Walsh F.S., and Doherty P. The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J. Cell Biol. 160 (2003) 481-486
102. Wilson R.I., Kunos G., and Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31 (2001) 453-462
103. Wilson R.I., and Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410 (2001) 588-592
104. Wisco D., Anderson E.D., Chang M.C., Norden C., Boiko T., Folsch H., and Winckler B. Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol. 162 (2003) 1317-1328