Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation

Progress in Lipid Research

Volumn 52, Issue 4, 2013, Pages 633-650

  Galve Roperh, Ismael ^a   Chiurchiù, Valerio ^b,c   Díaz Alonso, Javier ^a   Bari, Monica ^d   Guzmán, Manuel ^a   Maccarrone, Mauro ^c,e  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSITY OF TERAMO   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e UNIVERSITY CAMPUS BIO MEDICO   (Italy)

Author keywords

Cell commitment; Cell survival; Endocannabinoids; Membrane receptors; Niche cues; Protein kinases; Transcription factors

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLETHANOLAMINE ACID AMIDASE; ACYLGLYCEROL LIPASE; AMIDASE; ANANDAMIDE; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCINEURIN; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOCANNABINOID; FATTY ACID AMIDASE; FIBROBLAST GROWTH FACTOR; GLUTAMATE DECARBOXYLASE; GLYCOGEN SYNTHASE KINASE 3BETA; LIPOPROTEIN LIPASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; METABOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; NERVE GROWTH FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; UNINDEXED DRUG; VANILLOID RECEPTOR 1; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ADIPOCYTE; B LYMPHOCYTE; BONE METABOLISM; BONE REMODELING; BONE TURNOVER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EPIDERMIS CELL; IMMUNOCOMPETENT CELL; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; METABOLISM; MONOCYTE; NATURAL KILLER CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROTRANSMITTER RELEASE; OSSIFICATION; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TROPHOBLAST;

CANNABIS; CANNABIS SATIVA;

2-AG; 2-ARACHIDONOYLGLYCEROL; AEA; BDNF; BRAIN DERIVED NEUROTROPHIC FACTOR; CAMP RESPONSE ELEMENT-BINDING PROTEIN; CANNABIDIOL; CANNABIGEROL; CBD; CBG; CELL COMMITMENT; CELL SURVIVAL; CFU-GEMM; COLONY-FORMING UNIT: GRANULOCYTE, ERYTHROCYTE, MACROPHAGE, MEGAKARYOCYTE; COLONY-STIMULATING FACTORS; CREB; CSF; DAGL; DIACYLGLYCEROL LIPASE; ECB; ECS; EMBRYONIC STEM; ENDOCANNABINOID; ENDOCANNABINOID SYSTEM; ENDOCANNABINOIDS; ERK; ES; EXTRACELLULAR-SIGNALING REGULATED PROTEIN KINASE; FAAH; FATTY ACID AMIDE HYDROLASE; FGF; FIBROBLAST GROWTH FACTOR; GAD; GLUTAMATE DECARBOXYLASE; GLYCOGEN SYNTHASE KINA; GSK3Β; HEMATOPOIETIC PROGENITOR CELLS; HEMATOPOIETIC STEM CELLS; HPC; HSC; ICM; INNER CELL MASS; L1-CAM; L1-CELL ADHESION MOLECULE; MAGL; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MEMBRANE RECEPTORS; METABOTROPIC GLUTAMATE RECEPTORS; MGLUR; MONOACYLGLYCEROL LIPASE; MTORC1; N-ARACHIDONOYLETHANOLAMINE; N-OLEOYLETHANOLAMINE; N-PALMITOYLETHANOLAMINE; NCAM; NERVE GROWTH FACTOR; NEURAL CELL ADHESION MOLECULE; NEURAL PROGENITOR/STEM CELL; NGF; NICHE CUES; NP; OEA; PEA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTORS; PHOSPHOINOSITOL 3-KINASE; PI3K; PKA; PPARΓ; PROTEIN KINASE-A; PROTEIN KINASES; RANKL; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA-B LIGAND; SUBVENTRICULAR ZONE; SVZ; THC; TRANSCRIPTION FACTORS; VENTRICULAR ZONE; VESICULAR GLUTAMATE TRANSPORTER; VGLUT; VZ; Δ(9)-TETRAHYDROCANNABINOL;

ANIMALS; CANNABINOIDS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; NEURONS; RECEPTORS, CANNABINOID; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84885352658     PISSN: 01637827     EISSN: 18732194     Source Type: Journal    
DOI: 10.1016/j.plipres.2013.05.004     Document Type: Review

References (200)

1. M.A. Elsohly, and D. Slade Chemical constituents of marijuana: the complex mixture of natural cannabinoids Life Sci 78 2005 539 548 (Pubitemid 41653504)
2. A.A. Izzo, F. Borrelli, R. Capasso, V. Di Marzo, and R. Mechoulam Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb Trends Pharmacol Sci 30 2009 515 527
3. Y. Gaoni, and R. Mechoulam The isolation and structure of delta-l-tetrahydrocannabinol and other neutral cannabinoids from hashish J Am Chem Soc 93 1971 217 224
4. A.C. Howlett, L.C. Blume, and G.D. Dalton CB(1) cannabinoid receptors and their associated proteins Curr Med Chem 17 2010 1382 1393
5. A. Luchicchi, and M. Pistis Anandamide and 2-arachidonoylglycerol: pharmacological properties, functional features, and emerging specificities of the two major endocannabinoids Mol Neurobiol 46 2012 374 392
6. P.M. 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
7. I. Brown, M.G. Cascio, D. Rotondo, R.G. Pertwee, S.D. Heys, and K.W. Wahle Cannabinoids and omega-3/6 endocannabinoids as cell death and anticancer modulators Prog Lipid Res 52 2012 50 109
8. Y. Okamoto, J. Morishita, K. Tsuboi, T. Tonai, and N. Ueda Molecular characterization of a phospholipase D generating anandamide and its congeners J Biol Chem 279 2004 5298 5305 (Pubitemid 38220550)
9. Y.X. Sun, K. Tsuboi, Y. Okamoto, T. Tonai, M. Murakami, and I. Kudo Biosynthesis of anandamide and N-palmitoylethanolamine by sequential actions of phospholipase A2 and lysophospholipase D Biochem J 380 2004 749 756 (Pubitemid 38850516)
10. G.M. Simon, and B.F. Cravatt Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway J Biol Chem 281 2006 26465 26472 (Pubitemid 44401855)
11. G.M. Simon, and B.F. Cravatt Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of glycerophospho-N-acyl ethanolamine precursors in mouse brain J Biol Chem 283 2008 9341 9349
12. J. Liu, L. Wang, J. Harvey-White, D. Osei-Hyiaman, R. Razdan, and Q. Gong Biosynthetic pathway for anandamide Proc Natl Acad Sci USA 103 2006 13345 13350
13. T. Bisogno, A. Mahadevan, R. Coccurello, J.W. Chang, M. Allarà, and Y. Chen A novel fluorophosphonate inhibitor of the biosynthesis of the endocannabinoid 2-arachidonoylglycerol with potential anti-obesity effects Br J Pharmacol 169 2013 784 793
14. R.G. Pertwee, A.C. Howlett, M.E. Abood, S.P. Alexander, V. Di Marzo, and M.R. Elphick International union of basic and clinical pharmacology. LXXIX. cannabinoid receptors and their ligands: beyond CB and CB Pharmacol Rev 62 2010 588 631
15. R.G. Pertwee Targeting the endocannabinoid system with cannabinoid receptor agonists: pharmacological strategies and therapeutic possibilities Philos Trans R Soc Lond B Biol Sci 367 2012 3353 3363
16. V. Di Marzo, and L. De Petrocellis Why do cannabinoid receptors have more than one endogenous ligand? Philos Trans R Soc Lond B Biol Sci 367 2012 3216 3228
17. M. Maccarrone, S. Rossi, M. Bari, V. De Chiara, F. Fezza, and A. Musella Anandamide inhibits metabolism and physiological actions of 2- arachidonoylglycerol in the striatum Nat Neurosci 11 2008 152 159 (Pubitemid 351170502)
18. X.H. Yu, C.Q. Cao, G. Martino, C. Puma, A. Morinville, and S. St-Onge A peripherally restricted cannabinoid receptor agonist produces robust antinociceptive effects in rodent models of inflammatory and neuropathic pain Pain 151 2010 337 344
19. M. Bari, N. Battista, F. Fezza, A. Finazzi-Agro, and M. Maccarrone Lipid rafts control signaling of type-1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis J Biol Chem 280 2005 12212 12220
20. T.W. Klein Cannabinoid-based drugs as anti-inflammatory therapeutics Nat Rev Immunol 5 2005 400 411 (Pubitemid 40685989)
21. R. Pandey, K. Mousawy, M. Nagarkatti, and P. Nagarkatti Endocannabinoids and immune regulation Pharmacol Res 60 2009 85 92
22. E. Bisicchia, V. Chiurchiù, M.T. Viscomi, L. Latini, F. Fezza, and L. Battistini Activation of type-2 cannabinoid receptor inhibits neuroprotective and antiinflammatory actions of glucocorticoid receptor α: when one is better than two Cell Mol Life Sci 70 2013 2191 2204
23. M.T. Cencioni, V. Chiurchiù, G. Catanzaro, G. Borsellino, G. Bernardi, and L. Battistini Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors PLoS One 5 2010 e8688
24. M.D. Van Sickle, M. Duncan, P.J. Kingsley, A. Mouihate, P. Urbani, and K. Mackie Identification and functional characterization of brainstem cannabinoid CB2 receptors Science 310 2005 329 332 (Pubitemid 41457202)
25. B.G. Ramirez, C. Blazquez, T. Gomez del Pulgar, M. Guzman, and M.L. de Ceballos Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockage of microglial activation J Neurosci 25 2005 1904 1913 (Pubitemid 40289395)
26. J.L. Shoemaker, K.A. Seely, R.L. Reed, J.P. Crow, and P.L. Prather The CB2 cannabinoid agonist AM-1241 prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis when inititated at symptom onset J Neurochem 101 2007 87 98 (Pubitemid 46426470)
27. M.T. Viscomi, S. Oddi, L. Latini, N. Pasquariello, F. Florenzano, and G. Bernardi Selective CB2 receptor agonism protects central neurons from remote axotomy-induced apoptosis through the PI3K/Akt pathway J Neurosci 29 2009 4564 4570
28. B.K. Atwood, and K. Mackie CB2: a cannabinoid receptor with an identity crisis Br J Pharmacol 160 2010 467 479
29. R.S. Blumberg, B. Dittel, D. Hafler, M. von Herrath, and F.O. Nestle Unraveling the autoimmune translational research process layer by layer Nat Med 18 2012 35 41
30. T. Gutierrez, J.D. Crystal, A.M. Zvonok, A. Makriyannis, and A.G. Hohmann Self medication of a cannabinoid CB2 agonist in an animal model of neuropathic pain Pain 152 2011 1976 1987
31. J. Palazuelos, T. Aguado, M.R. Pazos, B. Julien, C. Carrasco, and E. Resel Microglial CB2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity Brain 132 2009 3152 3164
32. S.H. Ramirez, J. Hasko', A. Skuba, S. Fan, H. Dykstra, and R. McCormick Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions J Neurosci 32 2012 4004 4016
33. J. Guindon, and A.G. Hohmann Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain Br J Pharmacol 153 2008 319 334
34. L.S. Premkumar, and M. Abooj TRP channels and analgesia Life Sci 92 2013 415 424
35. A. Musella, V. De Chiara, S. Rossi, C. Prosperetti, G. Bernardi, and M. Maccarrone TRPV1 channels facilitate glutamatetransmission in the striatum Mol Cell Neurosci 2009 40 2009 89 97
36. V. Di Marzo, and L. De Petrocellis Endocannabinoids as regulators of transient receptor potential (TRP) channels: a further opportunity to develop new endocannabinoid-based therapeutic drugs Curr Med Chem 17 2010 1430 1449
37. K. Starowicz, S. Nigam, and V. Di Marzo Biochemistry and pharmacology of endovanilloids Pharmacol Ther 114 2007 13 33 (Pubitemid 46498161)
38. M. Pistis, and M. Melis From surface to nuclear receptors: the endocannabinoid family extends its assets Curr Med Chem 17 2010 1450 1467
39. A. Chicca, J. Marazzi, S. Nicolussi, and J. Gertsch Evidence for bidirectional endocannabinoid transport across cell membranes J Biol Chem 287 2012 34660 34682
40. N. Ueda, K. Katayama, Y. Kurahashi, M. Suzuki, H. Suzuki, and S. Yamamoto Enzymological and molecular biological studies on anandamide amidohydrolase Adv Exp Med Biol 469 1999 513 518
41. M. Kaczocha, S.T. Glaser, J. Chae, D.A. Brown, and D.G. Deutsch Lipid droplets are novel sites of N-acylethanolamine inactivation by fatty acid amide hydrolase-2 J Biol Chem 285 2010 2796 2806
42. K. Tsuboi, N. Takezaki, and N. Ueda The N-acetylethanolamine-hydrolysing acid amidase (NAAA) chem Biodiversity 4 2007 1914 1925 (Pubitemid 47377209)
43. J.L. Blankman, G.M. Simon, and B.F. Cravatt A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol Chem Biol 14 2007 1347 1356 (Pubitemid 350257008)
44. D. Navia-Paldanius, J.R. Savinainen, and J.T. Laitinen Biochemical and pharmacological characterization of human α/β-hydrolase domain containing 6 (ABHD6) and 12 (ABHD12) J Lipid Res 53 2012 2413 2424
45. J.R. Savinainen, S.M. Saario, and J.T. Laitinen The serine hydrolases MAGL, ABHD6 and ABHD12 as guardians of 2-arachidonoylglycerol signalling through cannabinoid receptors Acta Physiol (Oxf) 204 2012 267 276
46. C.A. Rouzer, and L.J. Marnett Endocannabinoid oxygenation by cyclooxygenases, lipoxygenases, and cytochromes P450: cross-talk between the eicosanoid and endocannabinoid signaling pathways Chem Rev 111 2011 5899 5921
47. P.E. Castillo, T.J. Younts, A.E. Chavez, and Y. Hashimotodani Endocannabinoid signaling and synaptic function Neuron 76 2012 70 81
48. A.J. Becker, E.A. McCulloch, and J.E. Till Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells Nature 197 1963 452 454
49. S. Sell Stem cell handbook 2004 Humana Press Totowa, New Jersey
50. J. Hipp, and A. Atala Sources of stem cells for regenerative medicine Stem Cell Rev 4 2008 3 11
51. P. Sartipy Advancing pluripotent stem cell culture: it is a matter of setting the standard Stem Cells Dev 22 2013 1159 1161
52. K. Takahashi, K. Tanabe, M. Ohnuki, M. Narita, T. Ichisaka, and K. Tomoda Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 2007 861 872 (Pubitemid 350138099)
53. B.C. Paria, and S.K. Dey Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation Chem Phys Lipids 108 2000 211 220
54. M. Maccarrone, M. De Felici, F.G. Klinger, N. Battista, F. Fezza, and E. Dainese Mouse blastocysts release a lipid which activates anandamide hydrolase in intact uterus Mol Hum Reprod 10 2004 215 221 (Pubitemid 38456025)
55. H. Wang, S.K. Dey, and M. Maccarrone Jekyll and Hyde: two faces of cannabinoid signaling in male and female fertility Endocr Rev 27 2006 427 448 (Pubitemid 44213226)
56. S. Jiang, Y. Fu, J. Williams, J. Wood, L. Pandarinathan, and S. Avraham Expression and function of cannabinoid receptors CB1 and CB2 and their cognate cannabinoid ligands in murine embryonic stem cells PLoS One 2 2007 e641
57. X. Sun, and S.K. Dey Aspects of endocannabinoid signaling inperiimplantation biology Mol Cell Endocrinol 286 2008 S3 S11
58. O.M. Habayeb, A.H. Taylor, S.C. Bell, D.J. Taylor, and J.C. Konje Expression of the endocannabinoid system in human first trimester placenta and its role in trophoblast proliferation Endocrinology 149 2008 5052 5060
59. M. Bari, M. Tedesco, N. Battista, N. Pasquariello, M. Pucci, and V. Gasperi Characterization of the endocannabinoid system in mouse embryonic stem cells Stem Cells Dev 20 2011 139 147
60. B.C. Paria, W. Ma, D.M. Andrenyak, P.C. Schmid, H.H. Schmid, and D.E. Moody Effects of cannabinoids on preimplantation mouse embryo development and implantation are mediated by brain-type cannabinoid receptors Biol Reprod 58 1998 1490 1495 (Pubitemid 28248766)
61. J. Wang, B.C. Paria, S.K. Dey, and D.R. Armant Stage-specific excitation of cannabinoid receptor exhibits differential effects on mouse embryonic development Biol Reprod 60 1999 839 844 (Pubitemid 29149367)
62. M. Maccarrone, M. De Felici, M. Bari, F. Klinger, G. Siracusa, and A. Finazzi-Agrò Down-regulation of anandamide hydrolase in mouse uterus by sex hormones Eur J Biochem 267 2000 2991 2997 (Pubitemid 30321346)
63. J. Nones, T.C. Spohr, D.R. Furtado, R.C. Sartore, B.S. Paulsen, and M.Z. Guimaranes Cannabinoids modulate cell survival in embryoid bodies Cell Biol Int 34 2010 399 408
64. H.A. Oh, S. Kwon, S. Choi, H. Shin, K.H. Yoon, and W.J. Kim Uncovering a role for endocannabinoid signaling in autophagy in preimplantation mouse embryos Mol Hum Reprod 19 2013 93 101
65. H. Wang, and S.K. Dey Lipid signaling in embryo implantation Prostaglandins Other Lipid Mediat 77 2005 84 102 (Pubitemid 41133418)
66. X. Sun, H. Xie, J. Yang, H. Wang, H.B. Bradshaw, and S.K. Dey Endocannabinoid signaling directs differentiation of trophoblast cell lineages and placentation Proc Natl Acad Sci USA 107 2010 16887 16892
67. M. Khare, A.H. Taylor, J.C. Konje, and S.C. Bell Delta9- tetrahydrocannabinol inhibits cytotrophoblast cell proliferation and modulates gene trascription Mol Hum Reprod 12 2006 321 333 (Pubitemid 43821795)
68. H. Wang, Y. Guo, D. Wang, P.J. Kingsley, L.J. Marnett, and S.K. Das Aberrant cannabinoid signaling impair oviductal transport of embryos Nat Med 10 2004 1074 1080 (Pubitemid 39424868)
69. T. Harkany, M. Guzman, I. Galve-Roperh, P. Berghuis, L.A. Devi, and K. Mackie The emerging functions of endocannabinoid signaling during CNS development Trends Pharmacol Sci 28 2007 83 92 (Pubitemid 46161836)
70. J. Diaz-Alonso, T. Aguado, C.S. Wu, J. Palazuelos, C. Hofmann, and P. Garcez The CB1 cannabinoid receptor drives corticospinal motor neuron differentiation through the Ctip2/Satb2 transcriptional regulation axis J Neurosci 32 2012 16651 16665
71. J. Fernandez-Ruiz, F. Berrendero, M.L. Hernandez, and J.A. Ramos The endogenous cannabinoid system and brain development Trends Neurosci 23 2000 14 20 (Pubitemid 30100308)
72. D. Piomelli The molecular logic of endocannabinoid signalling Nat Rev Neurosci 4 2003 873 884 (Pubitemid 37351427)
73. J. Palazuelos, T. Aguado, A. Egia, R. Mechoulam, M. Guzman, and I. Galve-Roperh Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation FASEB J 20 2006 2405 2407
74. M.B. Goncalves, P. Suetterlin, P. Yip, F. Molina-Holgado, D.J. Walker, and M.J. Oudin A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner Mol Cell Neurosci 38 2008 526 536
75. J. Palazuelos, Z. Ortega, J. Díaz-Alonso, M. Guzmán, and I. Galve-Roperh CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling J Biol Chem 287 2012 1198 1209
76. J. Begbie, P. Doherty, and A. Graham Cannabinoid receptor, CB1, expression follows neuronal differentiation in the early chick embryo J Anat 205 2004 213 218 (Pubitemid 39341578)
77. T. Vitalis, J. Laine, A. Simon, A. Roland, C. Leterrier, and Z. Lenkei The type 1 cannabinoid receptor is highly expressed in embryonic cortical projection neurons and negatively regulates neurite growth in vitro Eur J Neurosci 28 2008 1705 1718
78. S. Watson, D. Chambers, C. Hobbs, P. Doherty, and A. Graham The endocannabinoid receptor, CB1, is required for normal axonal growth and fasciculation Mol Cell Neurosci 38 2008 89 97
79. P. Maison, D.J. Walker, F.S. Walsh, G. Williams, and P. Doherty BDNF regulates neuronal sensitivity to endocannabinoids Neurosci Lett 467 2009 90 94
80. E. Keimpema, G. Tortoriello, A. Alpar, S. Capsoni, I. Arisi, and D. Calvigioni Nerve growth factor scales endocannabinoid signaling by regulating monoacylglycerol lipase turnover in developing cholinergic neurons Proc Natl Acad Sci USA 110 2013 1935 1940
81. P. Berghuis, A.M. Rajnicek, Y.M. Morozov, R.A. Ross, J. Mulder, and G.M. Urban Hardwiring the brain: endocannabinoids shape neuronal connectivity Science 316 2007 1212 1216 (Pubitemid 46880959)
82. J. Mulder, T. Aguado, E. Keimpema, K. Barabas, and C.J. Ballester Rosado Endocannabinoid signaling controls pyramidal cell specification and long-range axon patterning Proc Natl Acad Sci USA 105 2008 8760 8765 (Pubitemid 351987753)
83. C. Compagnucci, S. Di Siena, M.B. Bustamante, D. Di Giacomo, M. Di Tommaso, and M. Maccarrone Type-1 (CB1) cannabinoid receptor promotes neuronal differentiation and maturation of neural stem cells PLoS One 8 2013 e54271
84. S.M. Eggan, M.S. Lazarus, S.R. Stoyak, D.W. Volk, J.R. Glausier, and Z.J. Huang Cortical glutamic acid decarboxylase 67 deficiency results in lower cannabinoid 1 receptor messenger RNA expression: implications for schizophrenia Biol Psychiatry 71 2012 114 119
85. C. Blazquez, A. Chiarlone, O. Sagredo, T. Aguado, M.R. Pazos, and E. Resel Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease Brain 134 2011 119 136
86. T. Aguado, K. Monory, J. Palazuelos, N. Stella, B. Cravatt, and B. Lutz The endocannabinoid system drives neural progenitor proliferation FASEB J 19 2005 1704 1706 (Pubitemid 41429536)
87. M.J. Oudin, S. Gajendra, G. Williams, C. Hobbs, G. Lalli, and P. Doherty Endocannabinoids regulate the migration of subventricular zone-derived neuroblasts in the postnatal brain J Neurosci 31 2011 4000 4011
88. T. Aguado, E. Romero, K. Monory, J. Palazuelos, M. Sendtner, and G. Marsicano The CB1 cannabinoid receptor mediates excitotoxicity-induced neural progenitor proliferation and neurogenesis J Biol Chem 282 2007 23892 23898 (Pubitemid 47328042)
89. A. Rubio-Araiz, A. Arevalo-Martin, O. Gomez-Torres, B. Navarro-Galve, D. Garcia-Ovejero, and P. Suetterlin The endocannabinoid system modulates a transient TNF pathway that induces neural stem cell proliferation Mol Cell Neurosci 38 2008 374 380
90. S.A. Wolf, A. Bick-Sander, K. Fabel, P. Leal-Galicia, S. Tauber, and G. Ramirez-Rodriguez Cannabinoid receptor CB1 mediates baseline and activity-induced survival of new neurons in adult hippocampal neurogenesis Cell Commun Signal 8 2010 12
91. M. Reisenberg, P.K. Singh, G. Williams, and P. Doherty The diacylglycerol lipases: structure, regulation and roles in and beyond endocannabinoid signalling Philos Trans R Soc Lond B Biol Sci 367 2012 3264 3275
92. Y. Gao, D.V. Vasilyev, M.B. Goncalves, F.V. Howell, C. Hobbs, and M. Reisenberg Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice J Neurosci 30 2010 2017 2024
93. E.J. Williams, F.S. Walsh, and P. Doherty The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response J Cell Biol 160 2003 481 486 (Pubitemid 36254386)
94. D.J. Walker, P. Suetterlin, M. Reisenberg, G. Williams, and P. Doherty Down-regulation of diacylglycerol lipase-alpha during neural stem cell differentiation: identification of elements that regulate transcription J Neurosci Res 88 2010 735 745
95. K.M. Jung, G. Astarita, D. Thongkham, and D. Piomelli Diacylglycerol lipase-alpha and -beta control neurite outgrowth in neuro-2a cells through distinct molecular mechanisms Mol Pharmacol 80 2011 60 67
96. T. Aguado, J. Palazuelos, K. Monory, N. Stella, B. Cravatt, and B. Lutz The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells J Neurosci 26 2006 1551 1561 (Pubitemid 43237025)
97. A.C. Campos, Z. Ortega, J. Palazuelos, M.V. Fogaca, D.C. Aguiar, and J. Diaz-Alonso The anxiolytic effect of cannabidiol on chronically stressed mice depends on hippocampal neurogenesis: involvement of the endocannabinoid system Int J Neuropsychopharmacol 2013 1 13
98. A.C. Flint, R.S. Dammerman, and A.R. Kriegstein Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations Proc Natl Acad Sci USA 96 1999 12144 12149 (Pubitemid 29502872)
99. R. Nochi, T. Kato, J. Kaneko, Y. Itou, H. Kuribayashi, and S. Fukuda Involvement of metabotropic glutamate receptor 5 signaling in activity-related proliferation of adult hippocampal neural stem cells Eur J Neurosci 36 2012 2273 2283
100. S. Ge, D.A. Pradhan, G.L. Ming, and H. Song GABA sets the tempo for activity-dependent adult neurogenesis Trends Neurosci 30 2007 1 8 (Pubitemid 46001680)
101. L. Li, K.J. Bender, P.J. Drew, S.P. Jadhav, E. Sylwestrak, and D.E. Feldman Endocannabinoid signaling is required for development and critical period plasticity of the whisker map in somatosensory cortex Neuron 64 2009 537 549
102. D. Rueda, B. Navarro, A. Martinez-Serrano, M. Guzman, and I. Galve-Roperh The endocannabinoid anandamide inhibits neuronal progenitor cell differentiation through attenuation of the RAP1/B-RAF/ERK pathway J Biol Chem 277 2002 46645 46650 (Pubitemid 35417665)
103. K. Jin, L. Xie, S.H. Kim, S. Parmentier-Batteur, Y. Sun, and X.O. Mao Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice Mol Pharmacol 66 2004 204 208 (Pubitemid 38989476)
104. W. Jiang, Y. Zhang, L. Xiao, J. Van Cleemput, S.P. Ji, and G. Bai Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic- and antidepressant-like effects J Clin Invest 115 2005 3104 3116 (Pubitemid 41567575)
105. J. Diaz-Alonso, M. Guzman, and I. Galve-Roperh Endocannabinoids via CB1 receptors act as neurogenic niche cues during cortical development Philos Trans R Soc Lond B Biol Sci 367 2012 3229 3241
106. O. Gomez, A. Arevalo-Martin, D. Garcia-Ovejero, S. Ortega-Gutierrez, J.A. Cisneros, and G. Almazan The constitutive production of the endocannabinoid 2-arachidonoylglycerol participates in oligodendrocyte differentiation Glia 58 2010 1913 1927
107. M.I. Davis, J. Ronesi, and D.M. Lovinger 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 2003 48973 48980
108. P. Derkinderen, E. Valjent, M. Toutant, J.C. Corvol, H. Enslen, and C. Ledent Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus J Neurosci 23 2003 2371 2382 (Pubitemid 36368926)
109. G.D. Dalton, and A.C. Howlett Cannabinoid CB1 receptors transactivate multiple receptor tyrosine kinases and regulate serine/threonine kinases to activate ERK in neuronal cells Br J Pharmacol 165 2012 2497 2511
110. P.J. Stork, and J.M. Schmitt Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation Trends Cell Biol 12 2002 258 266 (Pubitemid 34634174)
111. I. Galve-Roperh, D. Rueda, T. Gomez Del Pulgar, G. Velasco, and M. Guzman Mechanism of extracellular signal-regulated kinase activation by the CB(1) cannabinoid receptor Mol Pharmacol 62 2002 1385 1392 (Pubitemid 35403833)
112. P. Berghuis, M.B. Dobszay, X. Wang, S. Spano, F. Ledda, and K.M. Sousa Endocannabinoids regulate interneuron migration and morphogenesis by transactivating the TrkB receptor Proc Natl Acad Sci USA 102 2005 19115 19120 (Pubitemid 43049575)
113. S. Trazzi, M. Steger, V.M. Mitrugno, R. Bartesaghi, and E. Ciani CB1 cannabinoid receptors increase neuronal precursor proliferation through AKT/glycogen synthase kinase-3beta/beta-catenin signaling J Biol Chem 285 2010 10098 10109
114. L. Callen, E. Moreno, P. Barroso-Chinea, D. Moreno-Delgado, A. Cortes, and J. Mallol Cannabinoid receptors CB1 and CB2 form functional heteromers in brain J Biol Chem 287 2012 20851 20865
115. F. Steindel, R. Lerner, M. Haring, S. Ruehle, G. Marsicano, and B. Lutz Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus J Neurochem 124 2013 795 807
116. K.D. Bromberg, A. Ma'ayan, S.R. Neves, and R. Iyengar Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth Science 320 2008 903 909 (Pubitemid 351929582)
117. B.J. Molyneaux, P. Arlotta, J.R. Menezes, and J.D. Macklis Neuronal subtype specification in the cerebral cortex Nat Rev Neurosci 8 2007 427 437 (Pubitemid 46789231)
118. J. Soltys, M. Yushak, and Y. Mao-Draayer Regulation of neural progenitor cell fate by anandamide Biochem Biophys Res Commun 400 2010 21 26
119. O. Gomez, A. Sanchez-Rodriguez, M. Le, C. Sanchez-Caro, F. Molina-Holgado, and E. Molina-Holgado Cannabinoid receptor agonists modulate oligodendrocyte differentiation by activating PI3K/Akt and the mammalian target of rapamycin (mTOR) pathways Br J Pharmacol 163 2011 1520 1532
120. P. Sutterlin, E.J. Williams, D. Chambers, K. Saraf, D. von Schack, and M. Reisenberg The molecular basis of the cooperation between EGF, FGF and eCB receptors in the regulation of neural stem cell function Mol Cell Neurosci 52 2013 20 30
121. G. Marsicano, S. Goodenough, K. Monory, H. Hermann, M. Eder, and A. Cannich CB1 cannabinoid receptors and on-demand defense against excitotoxicity Science 302 2003 84 88 (Pubitemid 37210691)
122. F. Polleux, K.L. Whitford, P.A. Dijkhuize, T. Vitalis, and A. Ghosh Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling Development 129 2002 3147 3160 (Pubitemid 34874289)
123. H. Fukumitsu, M. Ohtsuka, R. Murai, H. Nakamura, K. Itoh, and S. Furukawa Brain-derived neurotrophic factor participates in determination of neuronal laminar fate in the developing mouse cerebral cortex J Neurosci 26 2006 13218 13230 (Pubitemid 46011632)
124. T.A. Hwangpo, J.D. Jordan, P.K. Premsrirut, G. Jayamaran, J.D. Licht, and R. Iyengar 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 2012 13674 13685
125. E. Keimpema, K. Barabas, Y.M. Morozov, G. Tortoriello, M. Torii, and G. Cameron Differential subcellular recruitment of monoacylglycerol lipase generates spatial specificity of 2-arachidonoyl glycerol signaling during axonal pathfinding J Neurosci 30 2010 13992 14007
126. A. Argaw, G. Duff, N. Zabouri, B. Cecyre, N. Chaine, and H. Cherif Concerted action of CB1 cannabinoid receptor and deleted in colorectal cancer in axon guidance J Neurosci 31 2011 1489 1499
127. C.S. Wu, J. Zhu, J. Wager-Miller, S. Wang, D. O'Leary, and K. Monory Requirement of cannabinoid CB(1) receptors in cortical pyramidal neurons for appropriate development of corticothalamic and thalamocortical projections Eur J Neurosci 32 2010 693 706
128. M. Gomez, M.L. Hernandez, M.R. Pazos, R.M. Tolon, J. Romero, and J. Fernandez-Ruiz Colocalization of CB(1) receptors with L1 and GAP-43 in forebrain white matter regions during fetal rat brain development: evidence for a role of these receptors in axonal growth and guidance Neuroscience 153 2008 687 699
129. M. Endo, M.A. Antonyak, and R.A. Cerione Cdc42-mTOR signaling pathway controls Hes5 and Pax6 expression in retinoic acid-dependent neural differentiation J Biol Chem 284 2009 5107 5118
130. D. Psychoyos, B. Hungund, T. Cooper, and R.H. Finnell A cannabinoid analog of Delta9-tetrahydrocannabinol disrupts neural development in chick Birth Defects Res B Dev Reprod Toxicol 83 2008 477 488
131. I. Katona, and T.F. Freund Endocannabinoid signaling as a synaptic circuit breaker in neurological disease Nat Med 14 2008 923 930
132. M. Schneider Cannabis use in pregnancy and early life and its consequences: animal models Eur Arch Psychiatry Clin Neurosci 259 2009 383 393
133. D.K. Nomura, J.L. Blankman, G.M. Simon, K. Fujioka, R.S. Issa, and A.M. Ward Activation of the endocannabinoid system by organophosphorus nerve agents Nat Chem Biol 4 2008 373 378 (Pubitemid 351693991)
134. T. Fiskerstrand, D. H'Mida-Ben Brahim, S. Johansson, A. M'Zahem, B.I. Haukanes, and N. Drouot Mutations in ABHD12 cause the neurodegenerative disease PHARC: an inborn error of endocannabinoid metabolism Am J Hum Genet 87 2010 410 417
135. D. Jutras-Aswad, J.A. DiNieri, T. Harkany, and Y.L. Hurd Neurobiological consequences of maternal cannabis on human fetal development and its neuropsychiatric outcome Eur Arch Psychiatry Clin Neurosci 259 2009 395 412
136. D. Bhattacharya, A. Czechowicz, A.G. Ooi, D.J. Rossi, D. Bryder, and I.L. Weissman Niche recycling through division-independent egress of hematopoietic stem cells J Exp Med 206 2009 2837 2850
137. D.E. Wright, A.J. Wagers, A.P. Gulati, F.L. Johnson, and I.L. Weissman Physiological migration of hematopoietic stem and progenitor cells Science 294 2001 1933 1936 (Pubitemid 33101591)
138. J.L. Abkowitz, A.E. Robinson, S. Kale, M.W. Long, and J. Chen Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure Blood 102 2003 1249 1253 (Pubitemid 36988029)
139. P. Valk, S. Verbakel, Y. Vankan, S. Hol, S. Mancham, and R. Ploemacher Anandamide, a natural ligand for the peripheral cannabinoid receptor is a novel synergistic growth factor for haematopoietic cells Blood 90 1997 1448 1457 (Pubitemid 27355416)
140. M.A. Jorda, S.E. Verbakel, P.J.M. Valk, Y.V. Vankan-Berkhoudt, M. Maccarrone, and A. Finazzi-Agro Haematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol Blood 99 2002 2786 2793 (Pubitemid 34525366)
141. D. Patinkin, G. Milman, A. Breuer, E. Fride, and R. Mechoulam Endocannabinoids as positive or negative factors in hematopoietic cell migration and differentiation Eur J Pharmacol 595 2008 1 6
142. J. Palazuelos, N. Davoust, B. Julien, E. Hatterer, T. Aguado, and R. Mechoulam The CB(2) cannabinoid receptor controls myeloid progenitor trafficking: involvement in the pathogenesis of an animal model of multiple sclerosis J Biol Chem 283 2008 13320 13329
143. J. Hoggat, and L.M. Pelus Eicosanoid regulation of hematopoiesis and hematopoietic stem and progenitor trafficking Leukemia 24 2010 1993 2002
144. S. Jiang, Y. Fu, and H.K. Avraham Regulation of hematopoietic stem cell trafficking and mobilization by the endocannabinoid system Transfusion 51 Suppl. 4 2011 65S 71S
145. J.P. Pereira, J. An, Y. Xu, Y. Huang, and J.G. Cyster Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids Nat Immunol 10 2009 403 411
146. A. Scutt, and E.M. Williamson Cannabinoids stimulate fibroblastic colony formation by bone marrow cells indirectly via CB2 receptors Calcif Tissue Int 80 2007 50 59 (Pubitemid 46098877)
147. M.V. Catani, F. Fezza, S. Baldassarri, V. Gasperi, A. Bertoni, and N. Pasquariello Expression of the endocannabinoid system in the bi-potential HEL cell line: commitment to the megakaryoblastic lineage by 2-arachidonoylglycerol J Mol Med 87 2009 65 74
148. E.S. Graham, C.E. Angel, L.E. Schwarcz, P.T. Dunbar, and M. Glass Detailed characterization of CB2 receptor protein expression in peripheral blood immune cells from healthy volunteers using flow cytometry Int J Immunopathol Pharmacol 23 2010 25 34
149. G. Murison, C.B.H. Chubb, S. Maeda, M.A. Gemmell, and E. Huberman Cannabinoids induce incomplete maturation of cultured human leukemia cells Proc Natl Acad Sci USA 84 1987 5414 5418 (Pubitemid 17129013)
150. P. Carayon, J. Marchand, D. Dussossoy, J.M. Derocq, O. Jbilo, and A. Bord Modulation and functional involvement of CB2 peripheral cannabinoid receptors during B-cell differentiation Blood 92 1998 3605 3615 (Pubitemid 28525186)
151. 9-tetrahydrocannabinol triggers profound defects in T cell differentiation and function in fetal and postnatal stages of life, including decreased responsiveness to HIV antigens J Pharmacol Exp Ther 339 2011 607 617
152. M. Gokoh, S. Kishimoto, S. Oka, Y. Metani, and T. Sugiura 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, enhances the adhesion of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes FEBS Lett 579 2005 6473 6478 (Pubitemid 41612170)
153. M. Gokoh, S. Kishimoto, S. Oka, Y. Metani, and T. Sugiura 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces rapid actin polymerization in HL-60 cells differentiated into macrophage-like cells Biochem J 386 2005 583 589 (Pubitemid 40445884)
154. K. Paulsen, S. Tauber, J. Timm, N. Goelz, C. Dumrese, and A. Stolzing The cannabinoid receptors agonist WIN55212.2 inhibits macrophageal differentiation and alters expression and phosphorylation of cell cycle control proteins Cell Commun Signal 28 2011 9 33
155. J.M. Derocq, O. Jbilo, M. Bouaboula, M. Ségui, C. Clère, and P. Casellas Genomic and functional changes induced by the activation of the peripheral cannabinoid receptor CB2 in the promyelocytic cells HL-60. Possible involvement of the CB2 receptor in cell differentiation J Biol Chem 275 2000 15621 15628 (Pubitemid 30366856)
156. R. Kurihara, Y. Tohyama, S. Matsusaka, H. Naruse, E. Kinoshita, and T. Tsujioka 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 (Pubitemid 43855384)
157. K. Sugawara, T. Bíró, D. Tsuruta, B.I. Tóth, A. Kromminga, and N. Zákány Endocannabinoids limit excessive mast cell maturation and activation in human skin J Allergy Clin Immunol 129 2012 726 738
158. M.F. Gurish, and K.F. Austen Developmental origin and functional specialization of mast cell subsets Immunity 37 2012 25 33
159. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
160. V.L. Hegde, M. Nagarkatti, and P.S. Nagarkatti Cannabinoid receptor activation leads to massive mobilization of myeloid-derived suppressor cells with potent immunosuppressive properties Eur J Immunol 40 2010 3358 3371
161. Q.Q. Tang, and M.D. Lane Adipogenesis: from stem cell to adipocyte Annu Rev Biochem 81 2012 715 736
162. I. Matias, M.P. Gonthier, P. Orlando, V. Martiadis, L. De Petrocellis, and C. Cervino Regulation, function and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia J Clin Endocrinol Metab 91 2006 3171 3180 (Pubitemid 44271774)
163. V. Gasperi, F. Fezza, N. Pasquariello, M. Bari, S. Oddi, and A. Finazzi Agrò Endocannabinoids in adipocytes during differentiation and their role in glucose uptake Cell Mol Life Sci 64 2007 219 229 (Pubitemid 46155701)
164. M. Bensaid, M. Gary-Bobo, A. Esclangon, J.P. Maffrand, G. LeFur, and F. Oury-Donat The cannabinoid CB1 receptor antagonist SR141716 increases Acrp30 mRNA expression in adipose tissue of obese fa/fa rats and in cultured adipocyte cells Mol Pharmacol 63 2003 908 914 (Pubitemid 36368998)
165. S. Engeli, J. Bohnke, M. Feldpausch, K. Gorzelniak, J. Janke, and S. Batkai Activation of the peripheral endocannabinoid system in human obesity Diabetes 54 2005 2838 2843 (Pubitemid 41401077)
166. R. Roche, L. Hoareau, S. Bes-Houtmann, M.P. Gonthier, C. Laborde, and J.F. Baron Presence of the cannabinoid receptors, CB1 and CB2, in human omental and subcutaneous adipocytes Histochem Cell Biol 4 2007 1 11
167. C. Pagano, C. Pilon, A. Calcagno, R. Urbanet, M. Rossato, and G. Milan The endogenous cannabinoid system stimulates glucose uptake in human fat cells via phosphatidylinositol 3-kinase and calcium-dependent mechanisms J Clin Endocrinol Metab 92 2007 4810 4819 (Pubitemid 350223464)
168. M. Gary-Bobo, G. Elachouri, B. Scatton, G. Le Fur, F. Oury-Donat, and M. Bensaid The cannabinoid CB1 receptor antagonist rimonabant (SR141716) inhibits cell proliferation and increases markers of adipocyte maturation in cultured mouse 3T3 F442A preadipocytes Mol Pharmacol 69 2006 471 478 (Pubitemid 43121944)
169. L. Bellocchio, C. Cervino, V. Vicennati, R. Pasquali, and U. Pagotto Cannabinoid type 1 receptor: another arrow in the adipocytes' bow J Neuroendocrinol 20 2008 130 138 (Pubitemid 351559286)
170. M. Bouaboula, S. Hilairet, J. Marchand, L. Fajas, G. Le Fur, and P. Casellas Anandamide induced PPAR gamma transcriptional activation and 3T3-L1 preadipocyte differentiation Eur J Pharmacol 517 2005 174 181 (Pubitemid 40977892)
171. S. Karaliota, A. Siafaka-Kapadai, C. Gontinou, K. Psarra, and M. Mavri-Vavayanni Anandamide increases the differentiation of rat adipocytes and causes PPAR gamma and CB1 receptor upregulation Obesity (Silver Spring) 17 2009 1830 1838
172. O. Jbilo, C. Ravinet-Trillou, M. Arnone, I. Buisson, E. Bribes, and A. Péleraux The CB1 receptor antagonist rimonabant reverses the diet-induced obesity phenotype through the regulation of lipolysis and energy balance FASEB J 19 2005 1567 1569 (Pubitemid 41279033)
173. N. Perwitz, M. Fasshauer, and J. Klein Cannabinoid receptor signaling directly inhibits thermogenesis and alters expression of adiponectin and visfatin Horm Metab Res 38 2006 356 358 (Pubitemid 43864960)
174. R. Vettor, and C. Pagano The role of the endocannabinoid system in lipogenesis and fatty acid metabolism Best Pract Res Clin Endocrinol Metab 23 2009 51 63
175. G.G. Muccioli, D. Naslain, F. Bäckhed, C.S. Reigstad, D.M. Lambert, and N.M. Delzenne The endocannabinoid system links gut microbiota to adipogenesis Mol Syst Biol 6 2010 392
176. S. Takeda Central control of bone remodelling J Neuroendocrinol 20 2008 802 807 (Pubitemid 351858732)
177. K. Naylor, and R. Eastell Bone turnover markers: use in osteoporosis Nat Rev Rheumatol 8 2012 379 389
178. A.I. Idris, R.J. Van't Hof, I.R. Greig, S.A. Ridge, D. Baker, and R.A. Ross Regulation of bone mass, bone loss and osteoclast activity by cannabinoid receptors Nat Med 11 2005 774 779 (Pubitemid 41021210)
179. A.I. Idris, A. Sophocleous, E. Landao-Bassonga, M. Canals, G. Milligan, and D. Baker Cannabinoid receptor type 1 protects against age-related osteoporosis by regulating osteoblast and adipocyte differentiation in marrow stromal cells Cell Metab 10 2009 139 147
180. J.M. Gimble, S. Zvonic, Z.E. Floyd, M. Kassem, and M.E. Nuttall Playing with bone and fat J Cell Biochem 98 2006 251 266
181. J. Tam, O. Ofek, E. Fride, C. Ledent, Y. Gabet, and R. Müller Involvement of neuronal cannabinoid receptor CB1 in regulation of bone mass and bone remodelling Mol Pharmacol 70 2006 786 792 (Pubitemid 44268435)
182. O. Ofek, M. Karsak, N. Leclerc, M. Fogel, B. Frenkel, and K. Wright Peripheral cannabinoid receptor, CB2, regulates bone mass Proc Natl Acad Sci USA 103 2006 696 701 (Pubitemid 43153088)
183. A.I. Idris, A. Sophocleous, E. Landao-Bassonga, R.J. Van't Hof, and S.H. Ralston Regulation of bone mass, osteoclast function, and ovariectomy-induced bone loss by the type 2 cannabinoid receptor Endocrinology 149 2008 5619 5626
184. D.C. Geng, Y.Z. Xu, H.L. Yang, G.M. Zhu, X.B. Wang, and X.S. Zhu Cannabinoid receptor-2 selective antagonist negatively regulates receptor activator of nuclear factor kappa B ligand mediated osteoclastogenesis Chin Med J 124 2011 586 590
185. Z. Nemes, and P.M. Steinert Bricks and mortar of the epidermal barrier Exp Mol Med 31 1999 5 19 (Pubitemid 29164098)
186. A.C. Kendall, and A. Nicolaou Bioactive lipid mediators in skin inflammation and immunity Prog Lipid Res 52 2013 141 164
187. E. Candi, R. Schmidt, and G. Melino The cornified envelope: a model of cell death in the skin Nat Rev Mol Cell Biol 6 2005 328 340 (Pubitemid 40516899)
188. E. Fuchs, and D.W. Cleveland A structural scaffolding of intermediate filaments in health and disease Science 279 1998 514 519 (Pubitemid 28067272)
189. L. Lorand, and R.M. Graham Transglutaminases: crosslinking enzymes with pleiotropic functions Nat Rev Mol Cell Biol 4 2003 140 156 (Pubitemid 36172696)
190. M. Maccarrone, M. Di Rienzo, N. Battista, V. Gasperi, P. Guerrieri, and A. Rossi The endocannabinoid system in human keratinocytes. Evidence that anandamide inhibits epidermal differentiation through CB1 receptor-dependent inhibition of protein kinase C, activation protein-1, and transglutaminase J Biol Chem 278 2003 33896 33903 (Pubitemid 37553223)
191. A. Paradisi, N. Pasquariello, D. Barcaroli, and M. Maccarrone Anandamide regulates keratinocyte differentiation by inducing DNA methylation in a CB1 receptor-dependent manner J Biol Chem 283 2008 6005 6012
192. J.D. Wilkinson, and E.M. Williamson Cannabinoids inhibit human keratinocyte proliferation through a non-CB1/CB2 mechanism and have a potential therapeutic value in the treatment of psoriasis J Dermatol Sci 45 2007 87 92 (Pubitemid 46108487)
193. T. Roelandt, C. Heughebaert, S. Bredif, C. Giddelo, C. Baudouin, and P. Msika Cannabinoid receptors 1 and 2 oppositely regulate epidermal permeability barrier status and differentiation Exp Dermatol 21 2012 688 693
194. M.A. Jordà, B. Lowenberg, and R. Delwel The peripheral cannabinoid receptor Cb2, a novel oncoprotein, induces a reversible block in neutrophilic differentiation Blood 101 2003 1336 1343 (Pubitemid 36182504)
195. M.A. Jorda, N. Rayman, M. Tas, S.E. Verbakel, N. Battista, and K. Van Lom The peripheral cannabinoid receptor Cb2, frequently expressed on AML blasts, either produces a neutrophilic differentiation block or confers abnormal migration properties in a ligand-dependent manner Blood 104 2004 526 534 (Pubitemid 38900037)
196. M. Kokaia Seizure-induced neurogenesis in the adult brain Eur J Neurosci 33 2011 1133 1138
197. E. Butti, M. Bacigaluppi, S. Rossi, M. Cambiaghi, M. Bari, and A. Cebrian Silla Subventricular zone neural progenitors protect striatal neurons from glutamatergic excitotoxicity Brain 135 2012 3320 3335
198. K. Mackie Cannabinoid receptors as therapeutic targets Annu Rev Pharmacol Toxicol 46 2006 101 122 (Pubitemid 43271185)
199. J.G. Zarruk, D. Fernandez-Lopez, I. Garcia-Yebenes, M.S. Garcia-Gutierrez, J. Vivancos, and F. Nombela Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection Stroke 43 2012 211 219
200. A.J. Eisch, and D. Petrik Depression and hippocampal neurogenesis: a road to remission? Science 338 2012 72 75