Endocannabinoids via CB1 receptors act as neurogenic niche cues during cortical development

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1607, 2012, Pages 3229-3241

  Díaz Alonso, Javier ^a   Guzmán, Manuel ^a   Galve Roperh, Ismael ^a  

^a INSTITUTO RAMÓN Y CAJAL DE INVESTIGACIÓN SANITARIA IRYCIS   (Spain)

Author keywords

Cortical progenitor; Endocannabinoid signaling; Neurogenesis

Indexed keywords

EID: 84868125270     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0385     Document Type: Review

References (117)

1. Sur, M. & Rubenstein, J. L. 2005 Patterning and plasticity of the cerebral cortex. Science 310, 805-810. (doi:10.1126/science.1112070)
2. O'Leary, D. D., Chou, S. J. & Sahara, S. 2007 Area patterning of the mammalian cortex. Neuron 56, 252-269. (doi:10.1016/j.neuron.2007.10.010)
3. Guillemot, F., Molnar, Z., Tarabykin, V. & Stoykova, A. 2006 Molecular mechanisms of cortical differentiation. Eur. J. Neurosci. 23, 857-868. (doi:10.1111/j.1460-9568.2006.04626.x)
4. Miller, F. D. & Gauthier, A. S. 2007 Timing is everything: making neurons versus glia in the developing cortex. Neuron 54, 357-369. (doi:10.1016/j.neuron.2007.04.019)
5. Eiraku, M. & Sasai, Y. In press. Self-formation of layered neural structures in three-dimensional culture of ES cells. Curr. Opin. Neurobiol.
6. Jutras-Aswad, D., DiNieri, J. A., Harkany, T. & Hurd, Y. L. 2009 Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome. Eur. Arch. Psychiat. Clin. Neurosci. 259, 395-412. (doi:10.1007/s00406-009-0027-z)
7. D'Souza, D. C., Sewell, R. A. & Ranganathan, M. 2009 Cannabis and psychosis/schizophrenia: human studies. Eur. Arch. Psychiat. Clin. Neurosci. 259, 413-431. (doi:10.1007/s00406-009-0024-2)
8. Heifets, B. D. & Castillo, P. E. 2009 Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol. 71, 283-306. (doi:10.1146/annurev.physiol.010908.163149)
9. Sun, X. & Dey, S. K. 2008 Aspects of endocannabinoid signaling in periimplantation biology. Mol. Cell Endocrinol. 286(Suppl. 1), S3-S11. (doi:10.1016/j.mce.2008.01.002)
10. Jiang, S. et al. 2007 Expression and function of cannabinoid receptors CB1 and CB2 and their cognate cannabinoid ligands in murine embryonic stem cells. PLoS ONE 2, e641. (doi:10.1371/journal.pone.0000641)
11. Psychoyos, D., Hungund, B., Cooper, T. & Finnell, R. H. 2008 A cannabinoid analogue of D9-tetrahydrocannabinol disrupts neural development in chick. Birth Defects Res. B Dev. Reprod. Toxicol. 83, 477-488. (doi:10.1002/bdrb.20166)
12. Berrendero, F., GarciaGil, L., Hernandez, M. L., Romero, J., Cebeira, M., de Miguel, R., Ramos, J. A. & Fernández-Ruiz, J. J. 1998 Localization of mRNA expression and activation of signal transduction mechanisms for cannabinoid receptor in rat brain during fetal development. Development 125, 3179-3188.
13. Mulder, J. et al. 2008 Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc. Natl Acad. Sci. USA 105, 8760-8765. (doi:10.1073/pnas.0803545105)
14. Vitalis, T., Laine, J., Simon, A., Roland, A., Leterrier, C. & Lenkei, Z. 2008 The type 1 cannabinoid receptor is highly expressed in embryonic cortical projection neurons and negatively regulates neurite growth in vitro. Eur. J. Neurosci. 28, 1705-1718. (doi:10.1111/j.1460-9568.2008.06484.x)
15. Morozov, Y. M., Torii, M. & Rakic, P. 2009 Origin, early commitment, migratory routes, and destination of cannabinoid type 1 receptor-containing interneurons. Cereb. Cortex 19(Suppl. 1), i78-i89. (doi:10.1093/cercor/bhp028)
16. Katona, I., Urban, G.M., Wallace, M., Ledent, C., Jung, K. M., Piomelli, D., Mackie, K. & Freund, T. F. 2006 Molecular composition of the endocannabinoid system at glutamatergic synapses. J. Neurosci. 26, 5628-5637. (doi:10.1523/JNEUROSCI.0309-06.2006)
17. Lafourcade, M., Elezgarai, I., Mato, S., Bakiri, Y., Grandes, P. & Manzoni, O. J. 2007 Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS ONE 2, e709. (doi:10.1371/journal.pone.0000709)
18. Monory, K. et al. 2006 The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51, 455-466. (doi:10.1016/j.neuron.2006.07.006)
19. Morozov, Y. M. & Freund, T. F. 2003 Postnatal development of type 1 cannabinoid receptor immunoreactivity in the rat hippocampus. Eur. J. Neurosci. 18, 1213-1222. (doi:10.1046/j.1460-9568.2003.02852.x)
20. Berghuis, P. et al. 2005 Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor. Proc. Natl Acad. Sci. USA 102, 19115-19120. (doi:10.1073/pnas.0509494102)
21. Bodor, A. L., Katona, I., Nyiri, G., Mackie, K., Ledent, C., Hajos, N. & Freund, T. F. 2005 Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J. Neurosci. 25, 6845-6856. (doi:10.1523/JNEUROSCI.0442-05.2005)
22. Hashimotodani, Y., Ohno-Shosaku, T. & Kano, M. 2007 Endocannabinoids and synaptic function in the CNS. Neuroscientist 13, 127-137. (doi:10.1177/1073858406296716)
23. Mato, S., Del Olmo, E. & Pazos, A. 2003 Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur. J. Neurosci. 17, 1747-1754. (doi:10.1046/j.1460-9568.2003.02599.x)
24. Wang, X., Dow-Edwards, D., Keller, E. & Hurd, Y. L. 2003 Preferential limbic expression of the cannabinoid receptor mRNA in the human fetal brain. Neuroscience 118, 681-694. (doi:10.1016/S0306-4522(03)00020-4)
25. Zurolo, E., Iyer, A. M., Spliet, W. G., Van Rijen, P. C., Troost, D., Gorter, J. A. & Aronica, E. 2010 CB1 and CB2 cannabinoid receptor expression during development and in epileptogenic developmental pathologies. Neuroscience 170, 28-41. (doi:10.1016/j.neuroscience.2010.07.004)
26. Galve-Roperh, I., Palazuelos, J., Aguado, T. & Guzman, M. 2009 The endocannabinoid system and the regulation of neural development: potential implications in psychiatric disorders. Eur. Arch. Psychiat. Clin. Neurosci. 259, 371-382. (doi:10.1007/s00406-009-0028-y)
27. Aguado, T. et al. 2006 The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J. Neurosci. 26, 1551-1561. (doi:10.1523/JNEUROSCI.3101-05.2006)
28. Kowalczyk, T. et al. 2009 Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb. Cortex 19, 2439-2450. (doi:10.1093/cercor/bhn260)
29. Aguado, T. et al. 2005 The endocannabinoid system drives neural progenitor proliferation. FASEB J. 19, 1704-1706.
30. Jiang, W., Zhang, Y., Xiao, L., Van Cleemput, J., Ji, S. P., Bai, G. & Zhang, X. 2005 Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects. J. Clin. Invest. 115, 3104-3116. (doi:10.1172/JCI25509)
31. Begbie, J., Doherty, P. & Graham, A. 2004 Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo. J. Anat. 205, 213-218. (doi:10.1111/j.0021-8782.2004.00325.x)
32. Watson, S., Chambers, D., Hobbs, C., Doherty, P. & Graham, A. 2008 The endocannabinoid receptor, CB1, is required for normal axonal growth and fasciculation. Mol. Cell Neurosci. 38, 89-97. (doi:10.1016/j.mcn.2008.02.001)
33. Lam, C. S., Rastegar, S. & Strahle, U. 2006 Distribution of cannabinoid receptor 1 in the CNS of zebrafish. Neuroscience 138, 83-95. (doi:10.1016/j.neuroscience.2005.10.069)
34. Palazuelos, J., Aguado, T., Egia, A., Mechoulam, R., Guzman, M. & Galve-Roperh, I. 2006 Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J. 20, 2405-2407. (doi:10.1096/fj.06-6164fje)
35. Molina-Holgado, F., Rubio-Araiz, A., Garcia-Ovejero, D., Williams, R. J., Moore, J. D., Arevalo-Martin, A., Gómez-Torres, O. & Molina-Holgado, E. 2007 CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur. J. Neurosci. 25, 629-634. (doi:10.1111/j.1460-9568.2007.05322.x)
36. Gao, Y. et al. 2010 Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci. 30, 2017-2024. (doi:10.1523/JNEUROSCI.5693-09.2010)
37. Berghuis, P. et al. 2007 Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316, 1212-1216. (doi:10.1126/science.1137406)
38. Argaw, A. et al. 2011 Concerted action of CB1 cannabinoid receptor and deleted in colorectal cancer in axon guidance. J. Neurosci. 31, 1489-1499. (doi:10.1523/JNEUROSCI.4134-09.2011)
39. Jung, K. M., Astarita, G., Thongkham, D. & Piomelli, D. 2011 Diacylglycerol lipase-a and -b control neurite outgrowth in neuro-2a cells through distinct molecular mechanisms. Mol. Pharmacol. 80, 60-67. (doi:10.1124/mol.110.070458)
40. Goncalves, M. B. et al. 2008 A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol. Cell Neurosci. 38, 526-536. (doi:10.1016/j.mcn.2008.05.001)
41. Walker, D. J., Suetterlin, P., Reisenberg, M., Williams, G. & Doherty, P. 2010 Down-regulation of diacylglycerol lipase-alpha during neural stem cell differentiation: identification of elements that regulate transcription. J. Neurosci. Res. 88, 735-745.
42. Keimpema, E. et al. 2010 Differential subcellular recruitment of monoacylglycerol lipase generates spatial specificity of 2-arachidonoyl glycerol signaling during axonal pathfinding. J. Neurosci. 30, 13992-14007. (doi:10.1523/JNEUROSCI.2126-10.2010)
43. Jin, K., Xie, L., Kim, S. H., Parmentier-Batteur, S., Sun, Y., Mao, X. O., Childs, J. & Greenberg, D. A. 2004 Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol. Pharmacol. 66, 204-208. (doi:10.1124/mol.66.2.204)
44. Galve-Roperh, I., Aguado, T., Palazuelos, J. & Guzman, M. 2007 The endocannabinoid system and neurogenesis in health and disease. Neuroscientist 13, 109-114. (doi:10.1177/1073858406296407)
45. Trazzi, S., Steger, M., Mitrugno, V. M., Bartesaghi, R. & Ciani, E. 2010 CB1 cannabinoid receptors increase neuronal precursor proliferation through AKT/glycogen synthase kinase-3beta/beta-catenin signaling. J. Biol. Chem. 285, 10098-10109. (doi:10.1074/jbc.M109.043711)
46. Hwangpo, T. A., Jordan, J. D., Premsrirut, P. K., Jayamaran, G., Licht, J. D., Iyengar, R. & Neves, S. R. 2012 G-protein-regulated inducer of neurite outgrowth (GRIN) modulates Sprouty protein repression of mitogen-activated protein kinase (MAPK) activation by growth factor stimulation. J. Biol. Chem. 287, 13674-13685. (doi:10.1074/jbc.M111.320705)
47. Rueda, D., Navarro, B., Martinez-Serrano, A., Guzman, M. & Galve-Roperh, I. 2002 The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the RaP1/B-Raf/ERK pathway. J. Biol. Chem. 277, 46645-46650.
48. Galve-Roperh, I., Aguado, T., Palazuelos, J. & Guzman, M. 2008 Mechanisms of control of neuron survival by the endocannabinoid system. Curr. Pharm. Des. 14, 2279-2288. (doi:10.2174/138161208785740117)
49. Davis, M. I., Ronesi, J. & Lovinger, D. M. 2003 A predominant role for inhibition of the adenylate cyclase/protein kinase A pathway in ERK activation by cannabinoid receptor 1 in N1E-115 neuroblastoma cells. J. Biol. Chem. 278, 48973-48980. (doi:10.1074/jbc.M305697200)
50. Derkinderen, P., Valjent, E., Toutant, M., Corvol, J. C., Enslen, H., Ledent, C., Trzaskos, J., Caboche, J. & Girault, J. A. 2003 Regulation of extracellular signalregulated kinase by cannabinoids in hippocampus. J. Neurosci. 23, 2371-2382.
51. Galve-Roperh, I., Rueda, D., Gomez Del Pulgar, T., Velasco, G. & Guzman, M. 2002 Mechanism of extracellular signal-regulated kinase activation by the CB(1) cannabinoid receptor. Mol. Pharmacol. 62, 1385-1392. (doi:10.1124/mol.62.6.1385)
52. Dalton, G. D. & Howlett, A. C. 2012 Cannabinoid CB1 receptors transactivate multiple receptor tyrosine kinases and regulate serine/threonine kinases to activate ERK in neuronal cells. Br. J. Pharmacol. 165, 2497-2511. (doi:10.1111/j.1476-5381.2011.01455.x)
53. Hoeffer, C. A. & Klann, E. 2010 MTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 33, 67-75. (doi:10.1016/j.tins.2009.11.003)
54. Puighermanal, E., Marsicano, G., Busquets-Garcia, A., Lutz, B., Maldonado, R. & Ozaita, A. 2009 Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci. 12, 1152-1158. (doi:10.1038/nn.2369)
55. Puighermanal, E., Busquets-Garcia, A., Maldonado, R. & Uzaita, A. 2012 Cellular and intracellular mechanisms involved in the cognitive impairment of cannabinoids. Phil. Trans. R. Soc. B 367, 3254-3263. (doi:10.1098/rstb.2011.0384)
56. Palazuelos, J., Ortega, Z., Diaz-Alonso, J., Guzman, M. & Galve-Roperh, I. 2012 CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J. Biol. Chem. 287, 1198-1209. (doi:10.1074/jbc.M111.291294)
57. Zou, J. et al. 2011 Rheb1 is required for mTORC1 and myelination in postnatal brain development. Dev. Cell. 20, 97-108. (doi:10.1016/j.devcel.2010.11.020)
58. Gomez, O., Sanchez-Rodriguez, A., Le, M., Sanchez-Caro, C., Molina-Holgado, F. & Molina-Holgado, E. 2011 Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways. Br. J. Pharmacol. 163, 1520-1532. (doi:10.1111/j.1476-5381.2011.01414.x)
59. Carracedo, A. et al. 2006 The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell. 9, 301-312. (doi:10.1016/j.ccr.2006.03.005)
60. Salazar, M. et al. 2009 Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 119, 1359-1372. (doi:10.1172/JCI37948)
61. Callen, L. et al. 2012 Cannabinoid receptors CB1 and CB2 form functional heteromers in the brain. J. Biol. Chem. 287, 20851-20865.
62. Rozenfeld, R. et al. 2012 Receptor heteromerization expands the repertoire of cannabinoid signaling in rodent neurons. PLoS ONE 7, e29239. (doi:10.1371/journal.pone.0029239)
63. Marsicano, G. et al. 2002 The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530-534. (doi:10.1038/nature00839)
64. Aso, E., Ozaita, A., Valdizan, E. M., Ledent, C., Pazos, A., Maldonado, R. & Valverde, O. 2008 BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice. J. Neurochem. 105, 565-572. (doi:10.1111/j.1471-4159.2007.05149.x)
65. Bergami, M., Rimondini, R., Santi, S., Blum, R., Gotz, M. & Canossa, M. 2008 Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl Acad. Sci. USA 105, 15570-15575. (doi:10.1073/pnas.0803702105)
66. Hart, S., Fischer, O. M. & Ullrich, A. 2004 Cannabinoids induce cancer cell proliferation via tumor necrosis factor alpha-converting enzyme (TACE/ADAM17)-mediated transactivation of the epidermal growth factor receptor. Cancer Res. 64, 1943-1950. (doi:10.1158/0008-5472.CAN-03-3720)
67. Rubio-Araiz, A. et al. 2008 The endocannabinoid system modulates a transient TNF pathway that induces neural stem cell proliferation. Mol. Cell Neurosci. 38, 374-380. (doi:10.1016/j.mcn.2008.03.010)
68. Marsicano, G. et al. 2003 CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302, 84-88. (doi:10.1126/science.1088208)
69. Aguado, T., Romero, E., Monory, K., Palazuelos, J., Sendtner, M., Marsicano, G., Lutz, B., Guzman, M. & Galve-Roperh, I. 2007 The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis. J. Biol. Chem. 282, 23892-23898. (doi:10.1074/jbc.M700678200)
70. De March, Z. et al. 2008 Cortical expression of brain derived neurotrophic factor and type-1 cannabinoid receptor after striatal excitotoxic lesions. Neuroscience 152, 734-740. (doi:10.1016/j.neuroscience.2007.11.044)
71. Williams, E. J., Walsh, F. S. & Doherty, P. 2003 The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J. Cell Biol. 160, 481-486. (doi:10.1083/jcb.200210164)
72. Rueda, D., Navarro, B., Martinez-Serrano, A., Guzman, M. & Galve-Roperh, I. 2002 The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the Rap1/B-Raf/ERK pathway. J. Biol. Chem. 277, 46645-46650. (doi:10.1074/jbc.M206590200)
73. Ishii, I. & Chun, J. 2002 Anandamide-induced neuroblastoma cell rounding via the CB1 cannabinoid receptors. Neuroreport 13, 593-596. (doi:10.1097/00001756-200204160-00011)
74. Jordan, J. D. et al. 2005 Cannabinoid receptor-induced neurite outgrowth is mediated by Rap1 activation through G(alpha)o/i-triggered proteasomal degradation of Rap1GAPII. J. Biol. Chem. 280, 11413-11421. (doi:10.1074/jbc.M411521200)
75. Zhou, D. & Song, Z. H. 2001 CB1 cannabinoid receptormediated neurite remodeling in mouse neuroblastoma N1E-115 cells. J. Neurosci. Res. 65, 346-353. (doi:10.1002/jnr.1160)
76. He, J. C., Gomes, I., Nguyen, T., Jayaram, G., Ram, P. T., Devi, L. A. & Iyengar, R. 2005 The G alpha(o/i)-coupled cannabinoid receptor-mediated neurite outgrowth involves Rap regulation of Src and Stat3. J. Biol. Chem. 280, 33426-33434. (doi:10.1074/jbc.M502812200)
77. Zorina, Y., Iyengar, R. & Bromberg, K. D. 2010 Cannabinoid 1 receptor and interleukin-6 receptor together induce integration of protein kinase and transcription factor signaling to trigger neurite outgrowth. J. Biol. Chem. 285, 1358-1370. (doi:10.1074/jbc.M109.049841)
78. Smith, T. H., Sim-Selley, L. J. & Selley, D. E. 2010 Cannabinoid CB1 receptor-interacting proteins: novel targets for central nervous system drug discovery? Br. J. Pharmacol. 160, 454-466. (doi:10.1111/j.1476-5381.2010.00777.x)
79. Gomez, O. et al. 2010 The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation. Glia 58, 1913-1927. (doi:10.1002/glia.21061)
80. Arevalo-Martin, A., Garcia-Ovejero, D., Rubio-Araiz, A., Gomez, O., Molina-Holgado, F. & Molina-Holgado, E. 2007 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, 1548-1559. (doi:10.1111/j.1460-9568.2007.05782.x)
81. Bromberg, K. D., Ma'ayan, A., Neves, S. R. & Iyengar, R. 2008 Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth. Science 320, 903-909. (doi:10.1126/science.1152662)
82. Osumi, N., Shinohara, H., Numayama-Tsuruta, K. & Maekawa, M. 2008 Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26, 1663-1672. (doi:10.1634/stemcells.2007-0884)
83. Diaz-Alonso, J. et al. In press. The CBI cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis. J. Neurosci.
84. Molyneaux, B. J., Arlotta, P., Menezes, J. R. & Macklis, J. D. 2007 Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. (doi:10.1038/nrn2151)
85. Harkany, T., Guzman, M., Galve-Roperh, I., Berghuis, P., Devi, L. A. & Mackie, K. 2007 The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol. Sci. 28, 83-92. (doi:10.1016/j.tips.2006.12.004)
86. Molina-Holgado, E., Vela, J. M., Arevalo-Martin, A., Almazan, G., Molina-Holgado, F., Borrell, J. & Guaza, C. 2002 Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J. Neurosci. 22, 9742-9753.
87. Aguado, T., Carracedo, A., Julien, B., Velasco, G., Milman, G., Mechoulam, R., Alvarez, L., Guzmán, M. & Galve-Roperh, I. 2007 Cannabinoids induce glioma stem-like cell differentiation and inhibit gliomagenesis. J. Biol. Chem. 282, 6854-6862. (doi:10.1074/jbc.M608900200)
88. Fukuda, S., Abematsu, M., Mori, H., Yanagisawa, M., Kagawa, T., Nakashima, K., Yoshimura, A. & Taga, T. 2007 Potentiation of astrogliogenesis bySTAT3-mediated activation of bone morphogenetic protein-Smad signaling in neural stem cells. Mol. Cell Biol. 27, 4931-4937. (doi:10.1128/MCB.02435-06)
89. Pang, T., Atefy, R. & Sheen, V. 2008 Malformations of cortical development. Neurologist 14, 181-191. (doi:10.1097/NRL.0b013e31816606b9)
90. Sipe, J. C., Chiang, K., Gerber, A. L., Beutler, E. & Cravatt, B. F. 2002 A missense mutation in human fatty acid amide hydrolase associated with problem drug use. Proc. Natl Acad. Sci. USA 99, 8394-8399. (doi:10.1073/pnas.082235799)
91. Hariri, A. R., Gorka, A., Hyde, L. W., Kimak, M., Halder, I., Ducci, F., Ferrell, R. E., Goldman, D. & Manuck, S. B. 2009 Divergent effects of genetic variation in endocannabinoid signaling on human threat- and reward-related brain function. Biol. Psychiat. 66, 9-16. (doi:10.1016/j.biopsych.2008.10.047)
92. Fiskerstrand, T. et al. 2010 Mutations in ABHD12 cause the neurodegenerative disease PHARC: an inborn error of endocannabinoid metabolism. Am. J. Hum. Genet. 87, 410-417. (doi:10.1016/j.ajhg.2010.08.002)
93. Schneider, M. 2009 Cannabis use in pregnancy and early life and its consequences: animal models. Eur. Arch. Psychiat. Clin. Neurosci. 259, 383-393. (doi:10.1007/s00406-009-0026-0)
94. Wu, C. S., Zhu, J., Wager-Miller, J., Wang, S., O'Leary, D., Monory, K., Lutz, B., Mackie, K. & Lu, H.-C. 2010 Requirement of cannabinoid CB(1) receptors in cortical pyramidal neurons for appropriate development of corticothalamic and thalamocortical projections. Eur. J. Neurosci. 32, 693-706. (doi:10.1111/j.1460-9568.2010.07337.x)
95. Li, L., Bender, K. J., Drew, P. J., Jadhav, S. P., Sylwestrak, E. & Feldman, D. E. 2009 Endocannabinoid signaling is required for development and critical period plasticity of the whisker map in somatosensory cortex. Neuron 64, 537-549. (doi:10.1016/j.neuron.2009.10.005)
96. Ramocki, M. B. & Zoghbi, H. Y. 2008 Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455, 912-918. (doi:10.1038/nature07457)
97. Heng, J. I., Moonen, G. & Nguyen, L. 2007 Neurotransmitters regulate cell migration in the telencephalon. Eur. J. Neurosci. 26, 537-546. (doi:10.1111/j.1460-9568.2007.05694.x)
98. Martinez-Gras, I. et al. 2006 (AAT)n repeat in the cannabinoid receptor gene, CNR1: association with schizophrenia in a Spanish population. Eur. Arch. Psychiat. Clin. Neurosci. 256, 437-441. (doi:10.1007/s00406-006-0665-3)
99. Ponce, G., Hoenicka, J., Rubio, G., Ampuero, I., Jimenez-Arriero, M. A., Rodriguez-Jimenez, R., Palomo, T & Ramos, J. A., 2003 Association between cannabinoid receptor gene (CNR1) and childhood attention deficit/hyperactivity disorder in Spanish male alcoholic patients. Mol. Psychiat. 8, 466-467. (doi:10.1038/sj.mp.4001278)
100. Onaivi, E. S. et al. 2008 Brain neuronal CB2 cannabinoid receptors in drug abuse and depression: from mice to human subjects. PLoS ONE 3, e1640. (doi:10.1371/journal.pone.0001640)
101. Paz, R. D., Tardito, S., Atzori, M. & Tseng, K. Y. 2008 Glutamatergic dysfunction in schizophrenia: from basic neuroscience to clinical psychopharmacology. Eur. Neuropsychopharmacol. 18, 773-786. (doi:10.1016/j.euroneuro.2008.06.005)
102. Eggan, S. M., Hashimoto, T. & Lewis, D. A. 2008 Reduced cortical cannabinoid 1 receptor messenger RNA and protein expression in schizophrenia. Arch. Gen. Psychiat. 65, 772-784. (doi:10.1001/archpsyc.65.7.772)
103. Rakhade, S. N. & Jensen, F. E. 2009 Epileptogenesis in the immature brain: emerging mechanisms. Nat. Rev. Neurol. 5, 380-391. (doi:10.1038/nrneurol.2009.80)
104. Manent, J.B., Wang, Y., Chang, Y., Paramasivam, M. & LoTurco, J. J. 2009 Dcx reexpression reduces subcortical band heterotopia and seizure threshold in an animal model of neuronal migration disorder. Nat. Med. 15, 84-90. (doi:10.1038/nm.1897)
105. Nosten-Bertrand, M. et al. 2008 Epilepsy in Dcx knockout mice associated with discrete lamination defects and enhanced excitability in the hippocampus. PLoS ONE 3, e2473. (doi:10.1371/journal.pone.0002473)
106. Ludanyi, A. et al. 2008 Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J. Neurosci. 28, 2976-2990. (doi:10.1523/JNEUROSCI.4465-07.2008)
107. Chen, K. et al. 2003 Long-term plasticity of endocannabinoid signaling induced by developmental febrile seizures. Neuron 39, 599-611. (doi:10.1016/S0896-6273(03)00499-9)
108. Powell, E. M., Campbell, D. B., Stanwood, G. D., Davis, C., Noebels, J. L. & Levitt, P. 2003 Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J. Neurosci. 23, 622-631.
109. Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C. & Rubenstein, J. L. R. 2005 Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 8, 1059-1068. (doi:10.1038/nn1499)
110. Lodato, S. et al. 2011 Loss of COUP-TFI alters the balance between caudal ganglionic eminence- and medial ganglionic eminence-derived cortical interneurons and results in resistance to epilepsy. J. Neurosci. 31, 4650-4662. (doi:10.1523/JNEUROSCI.6580-10.2011)
111. Wyeth, M. S., Zhang, N., Mody, I. & Houser, C. R. 2010 Selective reduction of cholecystokinin-positive basket cell innervation in a model of temporal lobe epilepsy. J. Neurosci. 30, 8993-9006. (doi:10.1523/JNEUROSCI.1183-10.2010)
112. Antonucci, F. et al. 2012 Cracking down on inhibition: selective removal of GABAergic interneurons from hippocampal networks. J. Neurosci. 32, 1989-2001. (doi:10.1523/JNEUROSCI.2720-11.2012)
113. Cachope, R. 2012 Functional diversity of synaptic plasticity mediated by endocannabinoids. Phil. Trans. R. Soc. B 367, 3242-3253. (doi:10.1098/rstb.2011.0386)
114. Bernard, C., Milh, M., Morozov, Y. M., Ben-Ari, Y., Freund, T. F. & Gozlan, H. 2005 Altering cannabinoid signaling during development disrupts neuronal activity. Proc. Natl Acad. Sci. USA 102, 9388-9393. (doi:10.1073/pnas.0409641102)
115. Chen, K., Neu, A., Howard, A. L., Foldy, C., Echegoyen, J., Hilgenberg, L., Smith, M., Mackie, K. & Soltesz, I. 2007 Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J. Neurosci. 27, 46-58. (doi:10.1523/JNEUROSCI.3966-06.2007)
116. Katona, I. & Freund, T. F. 2008 Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat. Med. 14, 923-930. (doi:10.1038/nm.f.1869)
117. Lutz, B. & Monory, K. 2008 Soothing the seizures of children. Nat. Med. 14, 721-722. (doi:10.1038/nm0708-721)