Site-specific and time-dependent activation of the endocannabinoid system after transection of long-range projections

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Kallendrusch, Sonja ^a,b   Hobusch, Constance ^a   Ehrlich, Angela ^a   Ziebell, Simone ^c   Ueda, Natsuo ^d   Geisslinger, Gerd ^c   Koch, Marco ^a   Dehghani, Faramarz ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b Lipid Signaling Forschungszentrum   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; N ACYL PHOSPHATIDYLETHANOLAMINE SELECTIVE PHOSPHOLIPASE D; N ACYLETHANOLAMIDE HYDROLYZING ACID AMIDASE; N OLEOYLETHANOLAMINE; PALMIDROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CELL PROTECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEAFFERENTATION; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPAL CA1 REGION; LIQUID CHROMATOGRAPHY; MICROGLIA; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NERVE PROJECTION; NEWBORN; NONHUMAN; RAT; TANDEM MASS SPECTROMETRY; ANIMAL; CELL CULTURE; CELL DEATH; CYTOLOGY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; NERVE CELL; WESTERN BLOTTING; WISTAR RAT;

RATTUS;

ANIMALS; BLOTTING, WESTERN; CELL DEATH; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; ENDOCANNABINOIDS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; NEURONS; RATS; RATS, WISTAR; TANDEM MASS SPECTROMETRY;

EID: 84858735509     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033537     Document Type: Article

References (72)

1. Signoretti S, Vagnozzi R, Tavazzi B, Lazzarino G, (2010) Biochemical and neurochemical sequelae following mild traumatic brain injury: summary of experimental data and clinical implications. Neurosurg Focus 29: E1.
2. Dirnagl U, Iadecola C, Moskowitz MA, (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397.
3. Yakovlev AG, Faden AI, (2004) Mechanisms of neural cell death: implications for development of neuroprotective treatment strategies. NeuroRx 1: 5-16.
4. Faden AI, Stoica B, (2007) Neuroprotection: challenges and opportunities. Arch Neurol 64: 794-800.
5. Dumont RJ, Okonkwo DO, Verma S, Hurlbert RJ, Boulos PT, et al. (2001) Acute spinal cord injury, part I: pathophysiologic mechanisms. Clin Neuropharmacol 24: 254-264.
6. Piomelli D, (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4: 873-884.
7. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, et al. (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54: 161-202.
8. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI, (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346: 561-564.
9. Pertwee RG, Howlett AC, Abood ME, Alexander SP, Di Marzo V, et al. (2010) International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacol Rev 62: 588-631.
10. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, et al. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258: 1946-1949.
11. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, et al. (1995) 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215: 89-97.
12. Pertwee RG, (2010) Receptors and channels targeted by synthetic cannabinoid receptor agonists and antagonists. Curr Med Chem 17: 1360-1381.
13. 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: 5298-5305.
14. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, et al. (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384: 83-87.
15. Ueda N, (2002) Endocannabinoid hydrolases. Prostaglandins Other Lipid Mediat 68-69: 521-534.
16. Ueda N, Tsuboi K, Uyama T, (2010) N-acylethanolamine metabolism with special reference to N-acylethanolamine-hydrolyzing acid amidase (NAAA). Prog Lipid Res 49: 299-315.
17. Deller T, (1997) The anatomy of the rat fascia dentata-new vistas. Ann Anat 179: 501-504.
18. Frotscher M, Heimrich B, Deller T, (1997) Sprouting in the hippocampus is layer-specific. Trends Neurosci 20: 218-223.
19. Kovac AD, Kwidzinski E, Heimrich B, Bittigau P, Deller T, et al. (2004) Entorhinal cortex lesion in the mouse induces transsynaptic death of perforant path target neurons. Brain Pathol 14: 249-257.
20. Stoppini L, Buchs PA, Muller D, (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
21. Ramirez JJ, (2001) The role of axonal sprouting in functional reorganization after CNS injury: lessons from the hippocampal formation. Restor Neurol Neurosci 19: 237-262.
22. Brewer GJ, Torricelli JR, Evege EK, Price PJ, (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576.
23. Deller T, Del Turco D, Rappert A, Bechmann I, (2007) Structural reorganization of the dentate gyrus following entorhinal denervation: species differences between rat and mouse. Prog Brain Res 163: 501-528.
24. Bishay P, Schmidt H, Marian C, Haussler A, Wijnvoord N, et al. (2010) R-flurbiprofen reduces neuropathic pain in rodents by restoring endogenous cannabinoids. PLoS One 5: e10628.
25. Tsuboi K, Zhao LY, Okamoto Y, Araki N, Ueno M, et al. (2007) Predominant expression of lysosomal N-acylethanolamine-hydrolyzing acid amidase in macrophages revealed by immunochemical studies. Biochim Biophys Acta 1771: 623-632.
26. Zhao Y, Yuan Z, Liu Y, Xue J, Tian Y, et al. (2010) Activation of cannabinoid CB2 receptor ameliorates atherosclerosis associated with suppression of adhesion molecules. J Cardiovasc Pharmacol 55: 292-298.
27. Koch M, Kreutz S, Bottger C, Benz A, Maronde E, et al. (2011) Palmitoylethanolamide protects dentate gyrus granule cells via peroxisome proliferator-activated receptor-alpha. Neurotox Res 19: 330-340.
28. Kreutz S, Koch M, Ghadban C, Korf HW, Dehghani F, (2007) Cannabinoids and neuronal damage: differential effects of THC, AEA and 2-AG on activated microglial cells and degenerating neurons in excitotoxically lesioned rat organotypic hippocampal slice cultures. Exp Neurol 203: 246-257.
29. Kreutz S, Koch M, Bottger C, Ghadban C, Korf HW, et al. (2009) 2-Arachidonoylglycerol elicits neuroprotective effects on excitotoxically lesioned dentate gyrus granule cells via abnormal-cannabidiol-sensitive receptors on microglial cells. Glia 57: 286-294.
30. Grabiec U, Koch M, Kallendrusch S, Kraft R, Hill K, et al. (2011) The endocannabinoid N-arachidonoyldopamine (NADA) exerts neuroprotective effects after excitotoxic neuronal damage via cannabinoid receptor 1 (CB(1)). Neuropharmacology.
31. Koch M, Kreutz S, Bottger C, Grabiec U, Ghadban C, et al. (2011) The cannabinoid WIN 55,212-2-mediated protection of dentate gyrus granule cells is driven by CB1 receptors and modulated by TRPA1 and Ca(v) 2.2 channels. Hippocampus 21: 554-564.
32. Schuchmann S, Albrecht D, Heinemann U, von Bohlen und Halbach O, (2002) Nitric oxide modulates low-Mg2+-induced epileptiform activity in rat hippocampal-entorhinal cortex slices. Neurobiol Dis 11: 96-105.
33. Kovacs R, Rabanus A, Otahal J, Patzak A, Kardos J, et al. (2009) Endogenous nitric oxide is a key promoting factor for initiation of seizure-like events in hippocampal and entorhinal cortex slices. J Neurosci 29: 8565-8577.
34. Ziobro JM, Deshpande LS, Delorenzo RJ, (2011) An organotypic hippocampal slice culture model of excitotoxic injury induced spontaneous recurrent epileptiform discharges. Brain Res 1371: 110-120.
35. Bhaskaran MD, Smith BN, (2010) Cannabinoid-mediated inhibition of recurrent excitatory circuitry in the dentate gyrus in a mouse model of temporal lobe epilepsy. PLoS One 5: e10683.
36. Goffin K, Van Paesschen W, Van Laere K, (2011) In vivo activation of endocannabinoid system in temporal lobe epilepsy with hippocampal sclerosis. Brain 134: 1033-1040.
37. Hansen HH, Schmid PC, Bittigau P, Lastres-Becker I, Berrendero F, et al. (2001) Anandamide, but not 2-arachidonoylglycerol, accumulates during in vivo neurodegeneration. J Neurochem 78: 1415-1427.
38. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, et al. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302: 84-88.
39. Maccarrone M, Gubellini P, Bari M, Picconi B, Battista N, et al. (2003) Levodopa treatment reverses endocannabinoid system abnormalities in experimental parkinsonism. J Neurochem 85: 1018-1025.
40. Schabitz WR, Giuffrida A, Berger C, Aschoff A, Schwaninger M, et al. (2002) Release of fatty acid amides in a patient with hemispheric stroke: a microdialysis study. Stroke 33: 2112-2114.
41. Pisani A, Fezza F, Galati S, Battista N, Napolitano S, et al. (2005) High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson's disease patients. Ann Neurol 57: 777-779.
42. Eljaschewitsch E, Witting A, Mawrin C, Lee T, Schmidt PM, et al. (2006) The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49: 67-79.
43. Dommergues MA, Plaisant F, Verney C, Gressens P, (2003) Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection. Neuroscience 121: 619-628.
44. Franklin A, Parmentier-Batteur S, Walter L, Greenberg DA, Stella N, (2003) Palmitoylethanolamide increases after focal cerebral ischemia and potentiates microglial cell motility. J Neurosci 23: 7767-7775.
45. Conti S, Costa B, Colleoni M, Parolaro D, Giagnoni G, (2002) Antiinflammatory action of endocannabinoid palmitoylethanolamide and the synthetic cannabinoid nabilone in a model of acute inflammation in the rat. Br J Pharmacol 135: 181-187.
46. Rodriguez De Fonseca F, Gorriti MA, Bilbao A, Escuredo L, Garcia-Segura LM, et al. (2001) Role of the endogenous cannabinoid system as a modulator of dopamine transmission: implications for Parkinson's disease and schizophrenia. Neurotox Res 3: 23-35.
47. De Petrocellis L, Davis JB, Di Marzo V, (2001) Palmitoylethanolamide enhances anandamide stimulation of human vanilloid VR1 receptors. FEBS Lett 506: 253-256.
48. Raso GM, Esposito E, Vitiello S, Iacono A, Santoro A, et al. (2011) Palmitoylethanolamide stimulation induces allopregnanolone synthesis in C6 Cells and primary astrocytes: involvement of peroxisome-proliferator activated receptor-alpha. J Neuroendocrinol 23: 591-600.
49. Suardiaz M, Estivill-Torrus G, Goicoechea C, Bilbao A, Rodriguez de Fonseca F, (2007) Analgesic properties of oleoylethanolamide (OEA) in visceral and inflammatory pain. Pain 133: 99-110.
50. Fu J, Gaetani S, Oveisi F, Lo Verme J, Serrano A, et al. (2003) Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 425: 90-93.
51. Thabuis C, Tissot-Favre D, Bezelgues JB, Martin JC, Cruz-Hernandez C, et al. (2008) Biological functions and metabolism of oleoylethanolamide. Lipids 43: 887-894.
52. Galan-Rodriguez B, Suarez J, Gonzalez-Aparicio R, Bermudez-Silva FJ, Maldonado R, et al. (2009) Oleoylethanolamide exerts partial and dose-dependent neuroprotection of substantia nigra dopamine neurons. Neuropharmacology 56: 653-664.
53. Coffey PJ, Perry VH, Rawlins JN, (1990) An investigation into the early stages of the inflammatory response following ibotenic acid-induced neuronal degeneration. Neuroscience 35: 121-132.
54. Topper R, Gehrmann J, Schwarz M, Block F, Noth J, et al. (1993) Remote microglial activation in the quinolinic acid model of Huntington's disease. Exp Neurol 123: 271-283.
55. Hansen HS, (2010) Palmitoylethanolamide and other anandamide congeners. Proposed role in the diseased brain. Exp Neurol 224: 48-55.
56. Leung D, Saghatelian A, Simon GM, Cravatt BF, (2006) Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 45: 4720-4726.
57. Zhu C, Solorzano C, Sahar S, Realini N, Fung E, et al. (2011) Proinflammatory stimuli control N-acylphosphatidylethanolamine-specific phospholipase D expression in macrophages. Mol Pharmacol 79: 786-792.
58. Sun YX, Tsuboi K, Okamoto Y, Tonai T, Murakami M, et al. (2004) Biosynthesis of anandamide and N-palmitoylethanolamine by sequential actions of phospholipase A2 and lysophospholipase D. Biochem J 380: 749-756.
59. Simon GM, Cravatt BF, (2008) Anandamide biosynthesis catalyzed by the phosphodiesterase GDE1 and detection of glycerophospho-N-acyl ethanolamine precursors in mouse brain. J Biol Chem 283: 9341-9349.
60. Zhao LY, Tsuboi K, Okamoto Y, Nagahata S, Ueda N, (2007) Proteolytic activation and glycosylation of N-acylethanolamine-hydrolyzing acid amidase, a lysosomal enzyme involved in the endocannabinoid metabolism. Biochim Biophys Acta 1771: 1397-1405.
61. Maccarrone M, Piccirilli S, Battista N, Del Duca C, Nappi G, et al. (2004) Enhanced anandamide degradation is associated with neuronal apoptosis induced by the HIV-1 coat glycoprotein gp120 in the rat neocortex. J Neurochem 89: 1293-1300.
62. Degn M, Lambertsen KL, Petersen G, Meldgaard M, Artmann A, et al. (2007) Changes in brain levels of N-acylethanolamines and 2-arachidonoylglycerol in focal cerebral ischemia in mice. J Neurochem 103: 1907-1916.
63. Fowler CJ, Rojo ML, Rodriguez-Gaztelumendi A, (2010) Modulation of the endocannabinoid system: neuroprotection or neurotoxicity? Exp Neurol 224: 37-47.
64. Jin KL, Mao XO, Goldsmith PC, Greenberg DA, (2000) CB1 cannabinoid receptor induction in experimental stroke. Ann Neurol 48: 257-261.
65. De Petrocellis L, Chu CJ, Moriello AS, Kellner JC, Walker JM, et al. (2004) Actions of two naturally occurring saturated N-acyldopamines on transient receptor potential vanilloid 1 (TRPV1) channels. Br J Pharmacol 143: 251-256.
66. Lo Verme J, Fu J, Astarita G, La Rana G, Russo R, et al. (2005) The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol Pharmacol 67: 15-19.
67. Solorzano C, Zhu C, Battista N, Astarita G, Lodola A, et al. (2009) Selective N-acylethanolamine-hydrolyzing acid amidase inhibition reveals a key role for endogenous palmitoylethanolamide in inflammation. Proc Natl Acad Sci U S A 106: 20966-20971.
68. Nyilas R, Dudok B, Urban GM, Mackie K, Watanabe M, et al. (2008) Enzymatic machinery for endocannabinoid biosynthesis associated with calcium stores in glutamatergic axon terminals. J Neurosci 28: 1058-1063.
69. Zhang H, Hilton DA, Hanemann CO, Zajicek J, (2011) Cannabinoid Receptor and N-acyl Phosphatidylethanolamine Phospholipase D-Evidence for Altered Expression in Multiple Sclerosis. Brain Pathol.
70. Witting A, Walter L, Wacker J, Moller T, Stella N, (2004) P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc Natl Acad Sci U S A 101: 3214-3219.
71. Tham CS, Whitaker J, Luo L, Webb M, (2007) Inhibition of microglial fatty acid amide hydrolase modulates LPS stimulated release of inflammatory mediators. FEBS Lett 581: 2899-2904.
72. Nunez E, Benito C, Tolon RM, Hillard CJ, Griffin WS, et al. (2008) Glial expression of cannabinoid CB(2) receptors and fatty acid amide hydrolase are beta amyloid-linked events in Down's syndrome. Neuroscience 151: 104-110.