ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase

Journal of Neuroscience

Volumn 24, Issue 37, 2004, Pages 8068-8074

  Walter, Lisa ^a   Dinh, Thien ^b   Stella, Nephi ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

2 AG; Astrocyte; ATP; Cannabinoid; Glia; Lipase

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CANNABINOID; PURINE P2X RECEPTOR; PURINE RECEPTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; EXTRACELLULAR SPACE; GLIA CELL; MICROGLIA; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; ASTROCYTES; CALCIUM SIGNALING; CELLS, CULTURED; ENDOCANNABINOIDS; ENZYME ACTIVATION; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION PROFILING; GLYCERIDES; LIPOPROTEIN LIPASE; MICE; MICE, INBRED C57BL; MONOACYLGLYCEROL LIPASES; NERVE TISSUE PROTEINS; NEURONS; RECEPTORS, PURINERGIC P2; STIMULATION, CHEMICAL;

EID: 4644310682     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2419-04.2004     Document Type: Article

References (66)

1. Baker D, Pryce G, Croxford JL, Brown P, Pertwee RG, Makriyannis A, Khanolkar A, Layward L, Fezza F, Bisogno T, Di Marzo V (2001) Endocannabinoids control spasticity in a multiple sclerosis model. FASEB J 15:300-302.
2. Berdyshev EV, Schmid PC, Krebsbach RJ, Schmid HH (2001) Activation of PAF receptors results in enhanced synthesis of 2- arachidonoylglycerol (2-AG) in immune cells. FASEB J 15:2171-2178.
3. Bisogno T, Melck D, De Petrocellis L, Di Marzo V (1999a) Phosphatidic acid as the biosynthetic precursor of the endocannabinoid 2-arachidonoylglycerol in intact mouse neuroblastoma cells with ionomycin. J Neurochem 72:2213-2219.
4. Bisogno T, Berrendero F, Ambrosino G, Cebeira M, Ramos JA, Fernandez-Ruiz JJ, Di Marzo V (1999b) Brain regional distribution of endocannabinoids: implications for their biosynthesis and biological function. Biochem Biophys Res Commun 256:377-380.
5. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463-468.
6. Cabral GA, Harmon KN, Carlisle SJ (2001) Cannabinoid-mediated inhibition of inducible nitric oxide production by rat microglial cells: evidence for CB1 receptor participation. Adv Exp Med Biol 493:207-214.
7. 2 receptor-dependent mechanism. Mol Pharm 65:999-1007.
8. Chen Y, Swanson RA (2003) Astrocytes and brain injury. J Cereb Blood Flow Metab 23:137-149.
9. Chessell IP, Michel AD, Humphrey PP (1998) Effects of antagonists at the human recombinant P2X7 receptor. Br J Pharmacol 124:1314-1320.
10. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384:83-87.
11. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA 98:9371-9376.
12. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946-1949.
13. Di Marzo V, Hill MP, Bisogno T, Crossman AR, Brotchie JM (2000) Enhanced levels of endogenous cannabinoids in the globus pallidus are associated with a reduction in movement in an animal model of Parkinson's disease. FASEB J 14:1432-1438.
14. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819-10824.
15. Dubyak GR, El-Moatassim C (1993) Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 265:C577-606.
16. Edwards FA, Gibb AJ (1993) ATP -a fast neurotransmitter. FEBS Lett 325:86-89.
17. Ferrer B, Asbrock N, Kathuria S, Piomelli D, Giuffrida A (2003) Effects of levodopa on endocannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskinesias. Eur J Neurosci 18:1607-1614.
18. 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.
19. Fumagalli M, Brambilla R, D'Ambrosi N, Volonte C, Matteoli M, Verderio C, Abbracchio MP (2003) Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 43:218-230.
20. Gallily R, Breuer A, Mechoulam R (2000) 2-Arachidonylglycerol, an endogenous cannabinoid, inhibits tumor necrosis factor-alpha production in murine macrophages, and in mice. Eur J Pharmacol 406:5-7.
21. Goparaju SK, Ueda N, Yamaguchi H, Yamamoto S (1998) Anandamide amidohydrolase reacting with 2-arachidonoylglycerol, another cannabinoid receptor ligand. FEBS Lett 422:69-73.
22. Goparaju SK, Ueda N, Taniguchi K, Yamamoto S (1999) Enzymes of porcine brain hydrolyzing 2-arachidonoylglycerol, an endogenous ligand of cannabinoid receptors. Biochem Pharmacol 57:417-423.
23. Hansen HH, Schmid PC, Bittigau P, Lastres-Becker I, Berrendero F, Manzanares J, Ikonomidou C, Schmid HH, Fernandez-Ruiz JJ, Hansen HS (2001) Anandamide, but not 2-arachidonoylglycerol, accumulates during in vivo neurodegeneration. J Neurochem 78:1415-1427.
24. Hanus L, Avraham Y, Ben-Shushan D, Zolotarev O, Berry EM, Mechoulam R (2003) Short-term fasting and prolonged semistarvation have opposite effects on 2-AG levels in mouse brain. Brain Res 983:144-151.
25. Hoffman A, Kann O, Ohlemeyer C, Hanisch UK, Kettenmann H (2003) Elevation of basal intracellular calcium as a central element in the activation of brain macrophages (microglia): suppression of receptor-evoked calcium signaling and control of release function. J Neurosci 23:4410-4419.
26. Huang Z, Payette P, Abdullah K, Cromlish WA, Kennedy BP (1996) Functional identification of the active-site nucleophile of the human 85-kDa cytosolic phospholipase A2. Biochemistry 35:3712-3721.
27. James G, Butt AM (2002) P2Y and P2X purinoceptor mediated Ca(2+) signalling in glial cell pathology in the central nervous system. Eur J Pharmacol 447:247-260.
28. Jarai Z, Wagner JA, Varga K, Lake KD, Compton DR, Martin BR, Zimmer AM, Bonner TI, Buckley NE, Mezey E, Razdan RK, Zimmer A, Kunos G (1999) Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc Natl Acad Sci USA 96:14136-14141.
29. John GR, Simpson JE, Woodroofe MN, Lee SC, Brosnan CF (2001) Extracellular nucleotides differentially regulate interleukin-1beta signaling in primary human astrocytes: implications for inflammatory gene expression. J Neurosci 21:4134-4142.
30. Joseph SM, Buchakjian MR, Dubyak GR (2003) Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J Biol Chem 278:23331-23342.
31. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81.
32. Khaspekov LG, Brenz Verca MS, Frumkina LE, Hermann H, Marsicano G, Lutz B (2004) Involvement of brain-derived neurotrophic factor in cannabinoid receptor-dependent protection against excitotoxicity. Eur J Neurosci 19:1691-1698.
33. Khoo C, Helm J, Choi HB, Kim SU, McLarnon JG (2001) Inhibition of store-operated Ca(2+) influx by acidic extracellular pH in cultured human microglia. Glia 36:22-30.
34. Kishimoto S, Gokoh M, Oka S, Muramatsu M, Kajiwara T, Waku K, Sugiura T (2003) 2-arachidonoylglycerol induces the migration of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes through the cannabinoid CB2 receptor-dependent mechanism. J Biol Chem 278:24469-24475.
35. Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
36. Lio YC, Reynolds LJ, Balsinde J, Dennis EA (1996) Irreversible inhibition of Ca(2+)-independent phospholipase A2 by methyl arachidonyl fluorophosphonate. Biochim Biophys Acta 1302:55-60.
37. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
38. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stell M, Lopez-Rodriguez ML, Casanova E, Schutz G, Zieglgansberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88.
39. Matias I, Pochard P, Orlando P, Salzet M, Pestel J, Di Marzo V (2002) Presence and regulation of the endocannabinoid system in human dendritic cells. Eur J Biochem 269:3771-3778.
40. Moller T, Nolle C, Burger R, Verkhratsky A, Kellenmann H (1997) Mechanisms of C5a and C3a complement fragment-induced [Ca2+]i signaling in mouse microglia. J Neurosci 17:615-624.
41. Murgia M, Hanau S, Pizzo P, Rippa M, Di Virgilio F (1993) Oxidized ATP. An irreversible inhibitor of the macrophage purinergic P2Z receptor. J Biol Chem 268:8199-8203.
42. North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013-1067.
43. 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.
44. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R, Shohami E (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413:527-531.
45. Parmentier-Batteur S, Jin K, Mao XO, Xie L, Greenberg DA (2002) Increased severity of stroke in CB1 cannabinoid receptor knock-out mice. J Neurosci 22:9771-9775.
46. Shen M, Thayer SA (1998) Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol 54:459-462.
47. Shivachar AC, Martin BR, Ellis EF (1996) Anandamide- and delta9-tetrahydrocannabinol-evoked arachidonic acid mobilization and blockade by SR141716A [N-(Piperidin-1-yl)-5-(4-chlorophenyl)-1-(2,4-dichlorophenyl)-4- methyl-1H-pyrazole-3- carboximide hydrochloride]. Biochem Pharmacol 51:669-676.
48. Sinor AD, Irvin SM, Greenberg DA (2000) Endocannabinoids protect cerebral cortical neurons from in vitro ischemia in rats. Neurosci Lett 278:157-160.
49. Stella N, Piomelli D (2001) Receptor-dependent formation of endogenous cannabinoids in cortical neurons. Eur J Pharmacol 425:189-196.
50. Stella N, Pellerin L, Magistretti PJ (1995) Modulation of the glutamate-evoked release of arachidonic acid from mouse cortical neurons: involvement of a pH-sensitive membrane phospholipase A2. J Neurosci 15:3307-3317.
51. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
52. 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 215:89-97.
53. Sugiura T, Yoshinaga N, Kondo S, Waku K, Ishima Y (2000) Generation of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, in picrotoxinin-administered rat brain. Biochem Biophys Res Commun 271:654-658.
54. Sugiura T, Yoshinaga N, Waku K (2001) Rapid generation of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, in rat brain after decapitation. Neurosci Lett 297:175-178.
55. Sullivan JM (1999) Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82:1286-1294.
56. van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, Veldink GA, Vliegenthart JF, DiMarzo V, Nicolay K (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21:8765-8771.
57. van der Stelt M, Hansen HH, Veldhuis WB, Bar PR, Nicolay K, Veldink GA, Vliegenthart JFG, Hansen HS (2003) Biosynthesis of endocannabinoids and their modes of action in neurodegenerative diseases. Neurotox Res 5:183-200.
58. Waksman Y, Olson JM, Carlisle SJ, Cabral GA (1999) The central cannabinoid receptor (CB1) mediates inhibition of nitric oxide production by rat microglial cells. J Pharmacol Exp Ther 288:1357-1366.
59. Walter L, Stella N (2003) Endothelin-1 increases 2-arachidonoyl glycerol (2-AG) production in astrocytes. Glia 44:85-90.
60. Walter L, Stella N (2004) Cannabinoids and neuroinflammation. Br J Pharmacol 141:775-785.
61. Walter L, Franklin A, Witting A, Moller T, Stella N (2002) Astrocytes in culture produce anandamide and other acylethanolamides. J Biol Chem 26:26.
62. Walter L, Franklin A, Witting A, Wade C, Xie Y, Kunos G, Mackie K, Stella N (2003) Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J Neurosci 23:1398-1405.
63. Watanabe S, Doshi M, Hamazaki T (2003) n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice. Prostaglandins Leukot Essent Fatty Acids 69:51-59.
64. Wiley JS, Chen JR, Snook MB, Jamieson GP (1994) The P2Z-purinoceptor of human lymphocytes: actions of nucleotide agonists and irreversible inhibition by oxidized ATP. Br J Pharmacol 112:946-950.
65. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678-682.
66. Witting A, Walter L, Wacker J, Moller T, Stella N (2004) P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc Natl Acad Sci USA 101:3214-3219.