The evolution and comparative neurobiology of endocannabinoid signalling.
PDF (385K)
Journal: 2013/April - Philosophical Transactions of the Royal Society B: Biological Sciences
ISSN: 1471-2970
Abstract:
CB(1)- and CB(2)-type cannabinoid receptors mediate effects of the endocannabinoids 2-arachidonoylglycerol (2-AG) and anandamide in mammals. In canonical endocannabinoid-mediated synaptic plasticity, 2-AG is generated postsynaptically by diacylglycerol lipase alpha and acts via presynaptic CB(1)-type cannabinoid receptors to inhibit neurotransmitter release. Electrophysiological studies on lampreys indicate that this retrograde signalling mechanism occurs throughout the vertebrates, whereas system-level studies point to conserved roles for endocannabinoid signalling in neural mechanisms of learning and control of locomotor activity and feeding. CB(1)/CB(2)-type receptors originated in a common ancestor of extant chordates, and in the sea squirt Ciona intestinalis a CB(1)/CB(2)-type receptor is targeted to axons, indicative of an ancient role for cannabinoid receptors as axonal regulators of neuronal signalling. Although CB(1)/CB(2)-type receptors are unique to chordates, enzymes involved in biosynthesis/inactivation of endocannabinoids occur throughout the animal kingdom. Accordingly, non-CB(1)/CB(2)-mediated mechanisms of endocannabinoid signalling have been postulated. For example, there is evidence that 2-AG mediates retrograde signalling at synapses in the nervous system of the leech Hirudo medicinalis by activating presynaptic transient receptor potential vanilloid-type ion channels. Thus, postsynaptic synthesis of 2-AG or anandamide may be a phylogenetically widespread phenomenon, and a variety of proteins may have evolved as presynaptic (or postsynaptic) receptors for endocannabinoids.
Open in
PUBMED | DOI | PMC | Google Scholar | Wikipedia
Relations:
Content
Citations
(39)
References
(138)
Chemicals
(6)
Organisms
(2)
Processes
(3)
Anatomy
(2)
Affiliates
(1)
Similar articles
Articles by the same authors
Discussion board
Philos Trans R Soc Lond B Biol Sci 367(1607): 3201-3215
PMID: 23108540

The evolution and comparative neurobiology of endocannabinoid signalling

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
Email: ku.ca.lumq@kcihple.r.m
One contribution of 15 to a Theme Issue ‘Endocannabinoids in nervous system health and disease’.
School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
One contribution of 15 to a Theme Issue ‘Endocannabinoids in nervous system health and disease’.
Copyright This journal is © 2012 The Royal Society

Abstract

CB1- and CB2-type cannabinoid receptors mediate effects of the endocannabinoids 2-arachidonoylglycerol (2-AG) and anandamide in mammals. In canonical endocannabinoid-mediated synaptic plasticity, 2-AG is generated postsynaptically by diacylglycerol lipase alpha and acts via presynaptic CB1-type cannabinoid receptors to inhibit neurotransmitter release. Electrophysiological studies on lampreys indicate that this retrograde signalling mechanism occurs throughout the vertebrates, whereas system-level studies point to conserved roles for endocannabinoid signalling in neural mechanisms of learning and control of locomotor activity and feeding. CB1/CB2-type receptors originated in a common ancestor of extant chordates, and in the sea squirt Ciona intestinalis a CB1/CB2-type receptor is targeted to axons, indicative of an ancient role for cannabinoid receptors as axonal regulators of neuronal signalling. Although CB1/CB2-type receptors are unique to chordates, enzymes involved in biosynthesis/inactivation of endocannabinoids occur throughout the animal kingdom. Accordingly, non-CB1/CB2-mediated mechanisms of endocannabinoid signalling have been postulated. For example, there is evidence that 2-AG mediates retrograde signalling at synapses in the nervous system of the leech Hirudo medicinalis by activating presynaptic transient receptor potential vanilloid-type ion channels. Thus, postsynaptic synthesis of 2-AG or anandamide may be a phylogenetically widespread phenomenon, and a variety of proteins may have evolved as presynaptic (or postsynaptic) receptors for endocannabinoids.

Keywords: cannabinoid, anandamide, 2-AG, invertebrate, vertebrate, CRIP1a
Abstract

Acknowledgements

I am grateful to Dr Bradley Alger (University of Maryland, USA), Dr Brian Burrell (University of South Dakota, USA) and Dr Michaela Egertová (Queen Mary, University of London, UK) for commenting on and suggesting improvements to the manuscript during its preparation.

Acknowledgements

References

  • 1. Elphick M. R., Egertová M. 2001. The neurobiology and evolution of cannabinoid signalling. Phil. Trans. R. Soc. Lond. B356, 381–40810.1098/rstb.2000.0787 () ] [[PubMed]
  • 2. Wilson R. I., Nicoll R. A. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature410, 588–59210.1038/35069076 () [] [[PubMed]
  • 3. Kreitzer A. C., Regehr W. G. 2001. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron29, 717–72710.1016/S0896-6273(01)00246-X () [] [[PubMed]
  • 4. Ohno-Shosaku T., Maejima T., Kano M. 2001 Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron29, 729–73810.1016/S0896-6273(01)00247-1 () [] [[PubMed][Google Scholar]
  • 5. Egertová M., Giang D. K., Cravatt B. F., Elphick M. R. 1998. A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc. R. Soc. Lond. B265, 2081–208510.1098/rspb.1998.0543 () ] [[PubMed]
  • 6. Alger B. E. 2012. Endocannabinoids at the synapse a decade after the Dies Mirabilis (29 March 2001): what we still do not know. J. Physiol. 590, 2203–2212
  • 7. Pertwee R. G. 2005. Pharmacological actions of cannabinoids. Handb. Exp. Pharmacol.168, 1–5110.1007/3-540-26573-2_1 () [] [[PubMed]
  • 8. Devane W. A., Dysarz F. A., 3rd, Johnson M. R., Melvin L. S., Howlett A. C. 1988. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol.34, 605–613 [[PubMed]
  • 9. Matsuda L. A., Lolait S. J., Brownstein M. J., Young A. C., Bonner T. I. 1990. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature346, 561–56410.1038/346561a0 () [] [[PubMed]
  • 10. Munro S., Thomas K. L., Abu-Shaar M. 1993. Molecular characterization of a peripheral receptor for cannabinoids. Nature365, 61–6510.1038/365061a0 () [] [[PubMed]
  • 11. Ledent C., et al. 1999. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science283, 401–40410.1126/science.283.5400.401 () [] [[PubMed]
  • 12. Zimmer A., Zimmer A. M., Hohmann A. G., Herkenham M., Bonner T. I. 1999. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl Acad. Sci. USA96, 5780–578510.1073/pnas.96.10.5780 () ] [[PubMed]
  • 13. Buckley N. E., McCoy K. L., Mezey E., Bonner T., Zimmer A., Felder C. C., Glass M., Zimmer A. 2000. Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur. J. Pharmacol.396, 141–14910.1016/S0014-2999(00)00211-9 () [] [[PubMed]
  • 14. Devane W. A., et al. 1992. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science258, 1946–194910.1126/science.1470919 () [] [[PubMed]
  • 15. Mechoulam R., et al. 1995. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol.50, 83–9010.1016/0006-2952(95)00109-D () [] [[PubMed]
  • 16. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., Yamashita A., Waku K. 1995 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun.215, 89–9710.1006/bbrc.1995.2437 () [] [[PubMed][Google Scholar]
  • 17. Bisogno T., et al. 2003. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol.163, 463–46810.1083/jcb.200305129 () ] [[PubMed]
  • 18. Gao Y., et al. 2010. Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci.30, 2017–202410.1523/JNEUROSCI.5693-09.2010 () ] [[PubMed]
  • 19. Tanimura A., et al. 2010. The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron65, 320–32710.1016/j.neuron.2010.01.021 () [] [[PubMed]
  • 20. Dinh T. P., Carpenter D., Leslie F. M., Freund T. F., Katona I., Sensi S. L., Kathuria S., Piomelli D. 2002. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl Acad. Sci. USA99, 10 819–10 82410.1073/pnas.152334899 () ] [[PubMed]
  • 21. Schlosburg J. E., et al. 2010. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci.13, 1113–111910.1038/nn.2616 () ] [[PubMed]
  • 22. Long J. Z., et al. 2009. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat. Chem. Biol.5, 37–4410.1038/nchembio.129 () ] [[PubMed]
  • 23. Blankman J. L., Simon G. M., Cravatt B. F. 2007. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol.14, 1347–135610.1016/j.chembiol.2007.11.006 () ] [[PubMed]
  • 24. Schmid H. H. 2000. Pathways and mechanisms of N-acylethanolamine biosynthesis: can anandamide be generated selectively?Chem. Phys. Lipids108, 71–8710.1016/S0009-3084(00)00188-2 () [] [[PubMed]
  • 25. Cadas H., Gaillet S., Beltramo M., Venance L., Piomelli D. 1996 Biosynthesis of an endogenous cannabinoid precursor in neurons and its control by calcium and cAMP. J. Neurosci.16, 3934–3942 [Google Scholar]
  • 26. Schmid H. H., Schmid P. C., Natarajan V. 1990. N-acylated glycerophospholipids and their derivatives. Prog. Lipid Res.29, 1–4310.1016/0163-7827(90)90004-5 () [] [[PubMed]
  • 27. Okamoto Y., Morishita J., Tsuboi K., Tonai T., Ueda N. 2004 Molecular characterization of a phospholipase D generating anandamide and its congeners. J. Biol. Chem.279, 5298–530510.1074/jbc.M306642200 () [] [[PubMed][Google Scholar]
  • 28. Leung D., Saghatelian A., Simon G. M., Cravatt B. F. 2006. Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry45, 4720–472610.1021/bi060163l () ] [[PubMed]
  • 29. Egertová M., Simon G. M., Cravatt B. F., Elphick M. R. 2008. 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, 604–61510.1002/cne.21568 () [] [[PubMed]
  • 30. Simon G. M., Cravatt B. F. 2008. Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of glycerophospho-N-acyl ethanolamine precursors in mouse brain. J. Biol. Chem.283, 9341–934910.1074/jbc.M707807200 () ] [[PubMed]
  • 31. 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, 26 465–26 47210.1074/jbc.M604660200 () [] [[PubMed]
  • 32. Simon G. M., Cravatt B. F. 2010. Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo. Mol. Biosyst.6, 1411–141810.1039/c000237b () ] [[PubMed]
  • 33. Liu J., et al. 2008. Multiple pathways involved in the biosynthesis of anandamide. Neuropharmacology54, 1–710.1016/j.neuropharm.2007.05.020 () ] [[PubMed]
  • 34. Okamoto Y., Tsuboi K., Ueda N. 2009 Enzymatic formation of anandamide. Vitam. Horm.81, 1–2410.1016/S0083-6729(09)81001-7 () [] [[PubMed][Google Scholar]
  • 35. Tsuboi K., et al. 2011. Enzymatic formation of N-acylethanolamines from N-acylethanolamine plasmalogen through N-acylphosphatidylethanolamine-hydrolyzing phospholipase D-dependent and -independent pathways. Biochim. Biophys. Acta1811, 565–57710.1016/j.bbalip.2011.07.009 () [] [[PubMed]
  • 36. Cravatt B. F., Giang D. K., Mayfield S. P., Boger D. L., Lerner R. A., Gilula N. B. 1996. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature384, 83–8710.1038/384083a0 () [] [[PubMed]
  • 37. Cravatt B. F., Demarest K., Patricelli M. P., Bracey M. H., Giang D. K., Martin B. R., Lichtman A. H. 2001. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl Acad. Sci. USA98, 9371–937610.1073/pnas.161191698 () ] [[PubMed]
  • 38. Ahn K., et al. 2009. Discovery and characterization of a highly selective FAAH inhibitor that reduces inflammatory pain. Chem. Biol.16, 411–42010.1016/j.chembiol.2009.02.013 () ] [[PubMed]
  • 39. Wei B. Q., Mikkelsen T. S., McKinney M. K., Lander E. S., Cravatt B. F. 2006. A second fatty acid amide hydrolase with variable distribution among placental mammals. J. Biol. Chem.281, 36 569–36 57810.1074/jbc.M606646200 () [] [[PubMed]
  • 40. Kaczocha M., Glaser S. T., Chae J., Brown D. A., Deutsch D. G. 2010. Lipid droplets are novel sites of N-acylethanolamine inactivation by fatty acid amide hydrolase-2. J. Biol. Chem.285, 2796–280610.1074/jbc.M109.058461 () ] [[PubMed]
  • 41. Yu M., Ives D., Ramesha C. S. 1997. Synthesis of prostaglandin E2 ethanolamide from anandamide by cyclooxygenase-2. J. Biol. Chem.272, 21 181–21 18610.1074/jbc.272.34.21181 () [] [[PubMed]
  • 42. Kim J., Alger B. E. 2004. Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nat. Neurosci.7, 697–69810.1038/nn1262 () [] [[PubMed]
  • 43. Piomelli D., Beltramo M., Glasnapp S., Lin S. Y., Goutopoulos A., Xie X. Q., Makriyannis A. 1999. Structural determinants for recognition and translocation by the anandamide transporter. Proc. Natl Acad. Sci. USA96, 5802–580710.1073/pnas.96.10.5802 () ] [[PubMed]
  • 44. Glaser S. T., Abumrad N. A., Fatade F., Kaczocha M., Studholme K. M., Deutsch D. G. 2003. Evidence against the presence of an anandamide transporter. Proc. Natl Acad. Sci. USA100, 4269–427410.1073/pnas.0730816100 () ] [[PubMed]
  • 45. Fu J., et al. 2012. A catalytically silent FAAH-1 variant drives anandamide transport in neurons. Nat. Neurosci.15, 64–6910.1038/nn.2986 () ] [[PubMed]
  • 46. Premont R. T., Gainetdinov R. R. 2007. Physiological roles of G protein-coupled receptor kinases and arrestins. Annu. Rev. Physiol.69, 511–53410.1146/annurev.physiol.69.022405.154731 () [] [[PubMed]
  • 47. Metherell L. A., et al. 2005. Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nat. Genet.37, 166–17010.1038/ng1501 () [] [[PubMed]
  • 48. Cooray S. N., Almiro Do Vale I., Leung K. Y., Webb T. R., Chapple J. P., Egertová M., Cheetham M. E., Elphick M. R., Clark A. J. L. 2008. The melanocortin 2 receptor accessory protein exists as a homodimer and is essential for the function of the melanocortin 2 receptor in the mouse y1 cell line. Endocrinology149, 1935–194110.1210/en.2007-1463 () [] [[PubMed]
  • 49. Chan L. F., et al. 2009. MRAP and MRAP2 are bidirectional regulators of the melanocortin receptor family. Proc. Natl Acad. Sci. USA106, 6146–615110.1073/pnas.0809918106 () ] [[PubMed]
  • 50. Niehaus J. L., et al. 2007. CB1 cannabinoid receptor activity is modulated by the cannabinoid receptor interacting protein CRIP 1a. Mol. Pharmacol.72, 1557–156610.1124/mol.107.039263 () [] [[PubMed]
  • 51. Nie J., Lewis D. L. 2001. Structural domains of the CB1 cannabinoid receptor that contribute to constitutive activity and G-protein sequestration. J. Neurosci.21, 8758–8764
  • 52. Stauffer B., Wallis K. T., Wilson S. P., Egertová M., Elphick M. R., Lewis D. L., Hardy L. R. 2011. CRIP1a switches cannabinoid receptor agonist/antagonist-mediated protection from glutamate excitotoxicity. Neurosci. Lett.503, 224–22810.1016/j.neulet.2011.08.041 () [] [[PubMed]
  • 53. Piomelli D., Beltramo M., Giuffrida A., Stella N. 1998 Endogenous cannabinoid signaling. Neurobiol. Dis.5, 462–47310.1006/nbdi.1998.0221 () [] [[PubMed][Google Scholar]
  • 54. Herkenham M., Lynn A. B., de Costa B. R., Richfield E. K. 1991. Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res.547, 267–27410.1016/0006-8993(91)90970-7 () [] [[PubMed]
  • 55. Herkenham M., Lynn A. B., Johnson M. R., Melvin L. S., de Costa B. R., Rice K. C. 1991. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci.11, 563–583
  • 56. Matsuda L. A., Bonner T. I., Lolait S. J. 1993. Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neurol.327, 535–55010.1002/cne.903270406 () [] [[PubMed]
  • 57. Mailleux P., Vanderhaeghen J. J. 1992. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience48, 655–66810.1016/0306-4522(92)90409-U () [] [[PubMed]
  • 58. Tsou K., Brown S., Sanudo-Pena M. C., Mackie K., Walker J. M. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience83, 393–41110.1016/S0306-4522(97)00436-3 () [] [[PubMed]
  • 59. Pettit D. A., Harrison M. P., Olson J. M., Spencer R. F., Cabral G. A. 1998. Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J. Neurosci. Res.51, 391–40210.1002/(SICI)1097-4547(19980201)51:3<391::AID-JNR12>3.0.CO;2-A () [] [[PubMed]
  • 60. Roth S. H. 1978. Stereospecific presynaptic inhibitory effect of delta9-tetrahydrocannabinol on cholinergic transmission in the myenteric plexus of the guinea pig. Can. J. Physiol. Pharmacol.56, 968–97510.1139/y78-154 () [] [[PubMed]
  • 61. Stella N., Schweitzer P., Piomelli D. 1997 A second endogenous cannabinoid that modulates long-term potentiation. Nature388, 773–77810.1038/42015 () [] [[PubMed][Google Scholar]
  • 62. Yoshida T., Fukaya M., Uchigashima M., Miura E., Kamiya H., Kano M., Watanabe M. 2006 Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J. Neurosci.26, 4740–475110.1523/JNEUROSCI.0054-06.2006 () ] [[PubMed][Google Scholar]
  • 63. Gulyas A. I., Cravatt B. F., Bracey M. H., Dinh T. P., Piomelli D., Boscia F., Freund T. F. 2004. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur. J. Neurosci.20, 441–45810.1111/j.1460-9568.2004.03428.x () [] [[PubMed]
  • 64. Pan B., Wang W., Zhong P., Blankman J. L., Cravatt B. F., Liu Q. S. 2011. Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. J. Neurosci.31, 13 420–13 43010.1523/JNEUROSCI.2075-11.2011 () ] [[PubMed]
  • 65. Zhong P., Pan B., Gao X. P., Blankman J. L., Cravatt B. F., Liu Q. S. 2011. Genetic deletion of monoacylglycerol lipase alters endocannabinoid-mediated retrograde synaptic depression in the cerebellum. J. Physiol.589(Pt 20), 4847–485510.1113/jphysiol.2011.215509 () ] [[PubMed]
  • 66. Pan B., Wang W., Long J. Z., Sun D., Hillard C. J., Cravatt B. F., Liu Q.-S. 2009. Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4-(dibenzo[d][1,3]dioxol-5-yl(hydroxy)methyl)piperidine-1-carboxylate (JZL184) enhances retrograde endocannabinoid signaling. J. Pharmacol. Exp. Ther.331, 591–59710.1124/jpet.109.158162 () ] [[PubMed]
  • 67. Gerdeman G. L., Ronesi J., Lovinger D. M. 2002. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci.5, 446–451 [[PubMed]
  • 68. 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 ONE2, e709.10.1371/journal.pone.0000709 () ] [[PubMed]
  • 69. Grueter B. A., Brasnjo G., Malenka R. C. 2010. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci.13, 1519–152510.1038/nn.2685 () ] [[PubMed]
  • 70. Kim J., Alger B. E. 2010. Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat. Neurosci.13, 592–60010.1038/nn.2517 () ] [[PubMed]
  • 71. Chavez A. E., Chiu C. Q., Castillo P. E. 2010. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat. Neurosci.13, 1511–151810.1038/nn.2684 () ] [[PubMed]
  • 72. Onaivi E. S. 2011. Commentary: functional neuronal CB2 cannabinoid receptors in the CNS. Curr. Neuropharmacol.9, 205–20810.2174/157015911795017416 () ] [[PubMed]
  • 73. Elphick M. R., Egertová M. 2009. Cannabinoid receptor genetics and evolution. In The cannabinoid receptors (ed. Reggio P. H., editor. ), pp. 123–149 New York, NY: Humana Press [PubMed]
  • 74. Elphick M. R., Egertová M. 2005. The phylogenetic distribution and evolutionary origins of endocannabinoid signalling. Handb. Exp. Pharmacol.168, 283–29710.1007/3-540-26573-2_9 () [] [[PubMed]
  • 75. Elphick M. R. 2007. BfCBR: a cannabinoid receptor ortholog in the cephalochordate Branchiostoma floridae (Amphioxus). Gene399, 65–7110.1016/j.gene.2007.04.025 () [] [[PubMed]
  • 76. Elphick M. R., Satou Y., Satoh N. 2003. The invertebrate ancestry of endocannabinoid signalling: an orthologue of vertebrate cannabinoid receptors in the urochordate Ciona intestinalis. Gene302, 95–10110.1016/S0378-1119(02)01094-6 () [] [[PubMed]
  • 77. McPartland J. M., Glass M. 2003. Functional mapping of cannabinoid receptor homologs in mammals, other vertebrates, and invertebrates. Gene312, 297–30310.1016/S0378-1119(03)00638-3 () [] [[PubMed]
  • 78. McPartland J. M., Agraval J., Gleeson D., Heasman K., Glass M. 2006. Cannabinoid receptors in invertebrates. J. Evol. Biol.19, 366–37310.1111/j.1420-9101.2005.01028.x () [] [[PubMed]
  • 79. Karlsson M., Contreras J. A., Hellman U., Tornqvist H., Holm C. 1997. cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases. J. Biol. Chem.272, 27 218–27 22310.1074/jbc.272.43.27218 () [] [[PubMed]
  • 80. Hughes A. L., Irausquin S., Friedman R. 2010. The evolutionary biology of poxviruses. Infect. Genet. Evol.10, 50–5910.1016/j.meegid.2009.10.001 () ] [[PubMed]
  • 81. Song J., Kyriakatos A., El Manira A. 2012 Gating the polarity of endocannabinoid-mediated synaptic plasticity by nitric oxide in the spinal locomotor network. J. Neurosci.32, 5097–510510.1523/JNEUROSCI.5850-11.2012 () ] [[PubMed][Google Scholar]
  • 82. Thorn Perez C., Hill R. H., El Manira A., Grillner S. 2009. Endocannabinoids mediate tachykinin-induced effects in the lamprey locomotor network. J. Neurophysiol.102, 1358–136510.1152/jn.00294.2009 () [] [[PubMed]
  • 83. Kyriakatos A., El Manira A. 2007 Long-term plasticity of the spinal locomotor circuitry mediated by endocannabinoid and nitric oxide signaling. J. Neurosci.27, 12 664–12 67410.1523/JNEUROSCI.3174-07.2007 () ] [[PubMed][Google Scholar]
  • 84. Kettunen P., Kyriakatos A., Hallen K., El Manira A. 2005 Neuromodulation via conditional release of endocannabinoids in the spinal locomotor network. Neuron45, 95–10410.1016/j.neuron.2004.12.022 () [] [[PubMed][Google Scholar]
  • 85. Thompson J. A., Perkel D. J. 2011. Endocannabinoids mediate synaptic plasticity at glutamatergic synapses on spiny neurons within a basal ganglia nucleus necessary for song learning.J. Neurophysiol.105, 1159–116910.1152/jn.00676.2010 () ] [[PubMed]
  • 86. Cottone E., Forno S., Campantico E., Guastalla A., Viltono L., Mackie K., Franzoni M. F. 2005. Expression and distribution of CB1 cannabinoid receptors in the central nervous system of the African cichlid fish Pelvicachromis pulcher. J. Comp. Neurol.485, 293–30310.1002/cne.20502 () [] [[PubMed]
  • 87. Cesa R., Mackie K., Beltramo M., Franzoni M. F. 2001. Cannabinoid receptor CB1-like and glutamic acid decarboxylase-like immunoreactivities in the brain of Xenopus laevis. Cell Tissue Res.306, 391–39810.1007/s004410100461 () [] [[PubMed]
  • 88. Salio C., Cottone E., Conrath M., Franzoni M. F. 2002. CB1 cannabinoid receptors in amphibian spinal cord: relationships with some nociception markers. J. Chem. Neuroanat.24, 153–16210.1016/S0891-0618(02)00040-6 () [] [[PubMed]
  • 89. Soderstrom K., Tian Q. 2006 Developmental pattern of CB1 cannabinoid receptor immunoreactivity in brain regions important to zebra finch (Taeniopygia guttata) song learning and control. J. Comp. Neurol.496, 739–75810.1002/cne.20963 () [] [[PubMed][Google Scholar]
  • 90. Lam C. S., Rastegar S., Strahle U. 2006. Distribution of cannabinoid receptor 1 in the CNS of zebrafish. Neuroscience138, 83–9510.1016/j.neuroscience.2005.10.069 () [] [[PubMed]
  • 91. Cottone E., Campantico E., Guastalla A., Aramu S., Polzonetti-Magni A. M., Franzoni M. 2005. Are the cannabinoids involved in bony fish reproduction?Ann. N.Y. Acad. Sci.1040, 273–27610.1196/annals.1327.041 () [] [[PubMed]
  • 92. Hollis D. M., Coddington E. J., Moore F. L. 2006. Neuroanatomical distribution of cannabinoid receptor gene expression in the brain of the rough-skinned newt, Taricha granulosa. Brain Behav. Evol.67, 135–14910.1159/000090978 () [] [[PubMed]
  • 93. Stincic T. L., Hyson R. L. 2008. Localization of CB1 cannabinoid receptor mRNA in the brain of the chick (Gallus domesticus). Brain Res.1245, 61–7310.1016/j.brainres.2008.09.037 () ] [[PubMed]
  • 94. Alonso-Ferrero M. E., Paniagua M. A., Mostany R., Pilar-Cuellar F., Diez-Alarcia R., Pazos A., Fernández-López A., 2006. Cannabinoid system in the budgerigar brain. Brain Res.1087, 105–11310.1016/j.brainres.2006.02.119 () [] [[PubMed]
  • 95. Egertová M., Elphick M. R. 2000. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB1. J. Comp. Neurol.422, 159–17110.1002/(SICI)1096-9861(20000626)422:2<159::AID-CNE1>3.0.CO;2-1 () [] [[PubMed]
  • 96. Sanudo-Pena M. C., Romero J., Seale G. E., Fernandez-Ruiz J. J., Walker J. M. 2000. Activational role of cannabinoids on movement. Eur. J. Pharmacol.391, 269–27410.1016/S0014-2999(00)00044-3 () [] [[PubMed]
  • 97. Valenti M., Cottone E., Martinez R., De Pedro N., Rubio M., Viveros M. P., Franzoni M. F., Delgado M. J., Di Marzo V. 2005. The endocannabinoid system in the brain of Carassius auratus and its possible role in the control of food intake. J. Neurochem.95, 662–67210.1111/j.1471-4159.2005.03406.x () [] [[PubMed]
  • 98. Soderstrom K., Leid M., Moore F. L., Murray T. F. 2000. Behavioral, pharmacological, and molecular characterization of an amphibian cannabinoid receptor. J. Neurochem.75, 413–42310.1046/j.1471-4159.2000.0750413.x () [] [[PubMed]
  • 99. Soderstrom K., Johnson F. 2001 Zebra finch CB1 cannabinoid receptor: pharmacology and in vivo and in vitro effects of activation. J. Pharmacol. Exp. Ther.297, 189–197 [[PubMed][Google Scholar]
  • 100. Di Marzo V., Matias I. 2005 Endocannabinoid control of food intake and energy balance. Nat. Neurosci.8, 585–58910.1038/nn1457 () [] [[PubMed][Google Scholar]
  • 101. Soderstrom K., Tian Q., Valenti M., Di Marzo V. 2004 Endocannabinoids link feeding state and auditory perception-related gene expression. J. Neurosci.24, 10 013–10 02110.1523/JNEUROSCI.3298-04.2004 () ] [[PubMed][Google Scholar]
  • 102. Marsicano G., Lafenetre P. 2009 Roles of the endocannabinoid system in learning and memory. Curr. Top. Behav. Neurosci.1, 201–23010.1007/978-3-540-88955-7-8 () [] [[PubMed][Google Scholar]
  • 103. Clayton D. F. 1997. Role of gene regulation in song circuit development and song learning. J. Neurobiol.33, 549–57110.1002/(SICI)1097-4695(19971105)33:5<549::AID-NEU5>3.0.CO;2-4 () [] [[PubMed]
  • 104. Soderstrom K., Johnson F. 2003 Cannabinoid exposure alters learning of zebra finch vocal patterns. Brain Res. Dev. Brain Res.142, 215–21710.1016/S0165-3806(03)00061-0 () [] [[PubMed][Google Scholar]
  • 105. Soderstrom K., Tian Q. 2004 Distinct periods of cannabinoid sensitivity during zebra finch vocal development. Brain Res. Dev. Brain Res.153, 225–23210.1016/j.devbrainres.2004.09.002 () [] [[PubMed][Google Scholar]
  • 106. Soderstrom K., Johnson F. 2000 CB1 cannabinoid receptor expression in brain regions associated with zebra finch song control. Brain Res.857, 151–15710.1016/S0006-8993(99)02393-8 () [] [[PubMed][Google Scholar]
  • 107. Soderstrom K., Poklis J. L., Lichtman A. H. 2011. Cannabinoid exposure during zebra finch sensorimotor vocal learning persistently alters expression of endocannabinoid signaling elements and acute agonist responsiveness. BMC Neurosci.12, 3.10.1186/1471-2202-12-3 () ] [[PubMed]
  • 108. Soderstrom K., Luo B. 2010 Late-postnatal cannabinoid exposure persistently increases FoxP2 expression within zebra finch striatum. Dev. Neurobiol.70, 195–203 [Google Scholar]
  • 109. Gilbert M. T., Soderstrom K. 2011. Late-postnatal cannabinoid exposure persistently elevates dendritic spine densities in area X and HVC song regions of zebra finch telencephalon. Brain Res.1405, 23–3010.1016/j.brainres.2011.06.019 () ] [[PubMed]
  • 110. Whitney O., Soderstrom K., Johnson F. 2003 CB1 cannabinoid receptor activation inhibits a neural correlate of song recognition in an auditory/perceptual region of the zebra finch telencephalon. J. Neurobiol.56, 266–27410.1002/neu.10233 () ] [[PubMed][Google Scholar]
  • 111. Soderstrom K., Tian Q. 2008 CB(1) cannabinoid receptor activation dose dependently modulates neuronal activity within caudal but not rostral song control regions of adult zebra finch telencephalon. Psychopharmacology199, 265–27310.1007/s00213-008-1190-z () ] [[PubMed][Google Scholar]
  • 112. Schneider M. 2008 Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict. Biol.13, 253–26310.1111/j.1369-1600.2008.00110.x () [] [[PubMed][Google Scholar]
  • 113. Pertwee R. G., et al. 2010. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacol. Rev.62, 588–63110.1124/pr.110.003004 () ] [[PubMed]
  • 114. Egertová M., Elphick M. R. 2007. Localization of CiCBR in the invertebrate chordate Ciona intestinalis: evidence of an ancient role for cannabinoid receptors as axonal regulators of neuronal signalling. J. Comp. Neurol.502, 660–67210.1002/cne.21331 () [] [[PubMed]
  • 115. Matias I., McPartland J. M., Di Marzo V. 2005. Occurrence and possible biological role of the endocannabinoid system in the sea squirt Ciona intestinalis. J. Neurochem.93, 1141–115610.1111/j.1471-4159.2005.03103.x () [] [[PubMed]
  • 116. Schuel H., Goldstein E., Mechoulam R., Zimmerman A. M., Zimmerman S. 1994. Anandamide (arachidonylethanolamide), a brain cannabinoid receptor agonist, reduces sperm fertilizing capacity in sea urchins by inhibiting the acrosome reaction. Proc. Natl Acad. Sci. USA91, 7678–768210.1073/pnas.91.16.7678 () ] [[PubMed]
  • 117. Buznikov G. A., et al. 2010. A putative ‘pre-nervous’ endocannabinoid system in early echinoderm development.Dev. Neurosci. 32, 1–18
  • 118. Freeman R. M., Jr, et al. 2008. cDNA sequences for transcription factors and signaling proteins of the hemichordate Saccoglossus kowalevskii: efficacy of the expressed sequence tag (EST) approach for evolutionary and developmental studies of a new organism. Biol. Bull.214, 284–30210.2307/25470670 () [] [[PubMed]
  • 119. Sodergren E., et al. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science314, 941–95210.1126/science.1133609 () ] [[PubMed]
  • 120. Burke R. D., et al. 2006. A genomic view of the sea urchin nervous system. Dev. Biol.300, 434–46010.1016/j.ydbio.2006.08.007 () ] [[PubMed]
  • 121. Stefano G. B., Salzet B., Salzet M. 1997. Identification and characterization of the leech CNS cannabinoid receptor: coupling to nitric oxide release. Brain Res.753, 219–22410.1016/S0006-8993(96)01484-9 () [] [[PubMed]
  • 122. Elphick M. R. 1998. An invertebrate G-protein coupled receptor is a chimeric cannabinoid/melanocortin receptor. Brain Res.780, 168–17110.1016/S0006-8993(97)01297-3 () [] [[PubMed]
  • 123. Matias I., et al. 2001. Evidence for an endocannabinoid system in the central nervous system of the leech Hirudo medicinalis. Brain Res. Mol. Brain Res.87, 145–15910.1016/S0169-328X(00)00290-4 () [] [[PubMed]
  • 124. Li Q., Burrell B. D. 2009. Two forms of long-term depression in a polysynaptic pathway in the leech CNS: one NMDA receptor-dependent and the other cannabinoid-dependent. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol.195, 831–84110.1007/s00359-009-0462-3 () [] [[PubMed]
  • 125. Li Q., Burrell B. D. 2010. Properties of cannabinoid-dependent long-term depression in the leech. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol.196, 841–85110.1007/s00359-010-0566-9 () [] [[PubMed]
  • 126. Maione S., et al. 2006. 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, 969–98210.1124/jpet.105.093286 () [] [[PubMed]
  • 127. Yuan S., Burrell B. D. 2010. Endocannabinoid-dependent LTD in a nociceptive synapse requires activation of a presynaptic TRPV-like receptor. J. Neurophysiol.104, 2766–277710.1152/jn.00491.2010 () ] [[PubMed]
  • 128. Li Q., Burrell B. D. 2011. Associative, bidirectional changes in neural signaling utilizing NMDA receptor- and endocannabinoid-dependent mechanisms. Learn. Mem.18, 545–55310.1101/lm.2252511 () ] [[PubMed]
  • 129. Benjamin P. R., Kemenes G., Kemenes I. 2008. Non-synaptic neuronal mechanisms of learning and memory in gastropod molluscs. Front. Biosci.13, 4051–405710.2741/2993 () [] [[PubMed]
  • 130. Stefano G. B., Liu Y., Goligorsky M. S. 1996. Cannabinoid receptors are coupled to nitric oxide release in invertebrate immunocytes, microglia, and human monocytes. J. Biol. Chem.271, 19 238–19 24210.1074/jbc.271.32.19238 () [] [[PubMed]
  • 131. Sepe N., De Petrocellis L., Montanaro F., Cimino G., Di Marzo V. 1998 Bioactive long chain N-acylethanolamines in five species of edible bivalve molluscs. Possible implications for mollusc physiology and sea food industry. Biochim. Biophys. Acta1389, 101–11110.1016/S0005-2760(97)00132-X () [] [[PubMed][Google Scholar]
  • 132. Moroz L. L, et al. 2006. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell127, 1453–146710.1016/j.cell.2006.09.052 () ] [[PubMed]
  • 133. Fleury E., et al. 2009. Generation and analysis of a 29,745 unique expressed sequence tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the GigasDatabase. BMC Genomics10, 341.10.1186/1471-2164-10-341 () ] [[PubMed]
  • 134. Lehtonen M., Reisner K., Auriola S., Wong G., Callaway J. C. 2008. Mass-spectrometric identification of anandamide and 2-arachidonoylglycerol in nematodes. Chem. Biodivers.5, 2431–244110.1002/cbdv.200890208 () [] [[PubMed]
  • 135. Lucanic M., Held J. M., Vantipalli M. C., Klang I. M., Graham J. B., Gibson B. W., Lithgow G. J., Gill M. S. 2011. N-acylethanolamine signalling mediates the effect of diet on lifespan in Caenorhabditis elegans. Nature473, 226–22910.1038/nature10007 () ] [[PubMed]
  • 136. Montell C. 2012 Drosophila visual transduction. Trends Neurosci.413, 186–193 [PubMed][Google Scholar]
  • 137. Leung H. T., Tseng-Crank J., Kim E., Mahapatra C., Shino S., Zhou Y., An L., Doerge R. W., Pak W. L. 2008. DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron58, 884–89610.1016/j.neuron.2008.05.001 () ] [[PubMed]
  • 138. De Petrocellis L., Melck D., Bisogno T., Milone A., Di Marzo V. 1999 Finding of the endocannabinoid signalling system in Hydra, a very primitive organism: possible role in the feeding response. Neuroscience92, 377–38710.1016/S0306-4522(98)00749-0 () [] [[PubMed][Google Scholar]
  • 139. Chapman J. A, et al. 2010. The dynamic genome of Hydra. Nature464, 592–59610.1038/nature08830 () ] [[PubMed]
  • 140. Putnam N. H., et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science317, 86–94 ([PubMed]
Collaboration tool especially designed for Life Science professionals.Drag-and-drop any entity to your messages.