Immunohistochemical localization of anabolic and catabolic enzymes for anandamide and other putative endovanilloids in the hippocampus and cerebellar cortex of the mouse brain

Neuroscience

Volumn 151, Issue 4, 2008, Pages 955-968

  Cristino, L ^a   Starowicz, K ^a   De Petrocellis, L ^a   Morishita, J ^b   Ueda, N ^b   Guglielmotti, V ^a   Di Marzo, V ^a  

^a CNR   (Italy)

^b KAGAWA UNIVERSITY   (Japan)

Author keywords

anandamide; endovanilloid; FAAH; lipoxygenase; NADA; TRPV1

Indexed keywords

ACYLDOPAMINE; ANANDAMIDE; ARACHIDONATE 12 LIPOXYGENASE; CATECHOL METHYLTRANSFERASE; CYCLOOXYGENASE 2; DOPAMINE DERIVATIVE; ETHANOLAMINE DERIVATIVE; FATTY ACID AMIDASE; N ACYL PHOSPHATIDYLETHANOLAMINE; PEROXIDASE; PHOSPHOLIPASE D; UNCLASSIFIED DRUG; VANILLOID RECEPTOR; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CATABOLISM; CEREBELLUM CORTEX; CONTROLLED STUDY; ENZYME DEGRADATION; HIPPOCAMPUS; HISTOLOGY; HYDROLYSIS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMIDOHYDROLASES; ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; CATECHOL O-METHYLTRANSFERASE; CEREBELLAR CORTEX; CYCLOOXYGENASE 2; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; MALE; MICE; NEURONS; PHOSPHOLIPASE D; TRPV CATION CHANNELS;

EID: 39149131360     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.11.047     Document Type: Article

References (70)

1. Ahluwalia J.Y.M., Urban L., Bevan S., and Nagy I. Activation of capsaicin-sensitive primary sensory neurones induces anandamide production and release. J Neurochem 84 (2003) 585-591
2. Al-Hayani A., Wease K.N., Ross R.A., Pertwee R.G., and Davies S.N. The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology 41 (2001) 1000-1005
3. Benninger F., Freund T.F., and Hajois N. Control of excitatory synaptic transmission by capsaicin is unaltered in TRPV(1) vanilloid receptor knockout mice. Neurochem Int 52 (2008) 89-94
4. Bisogno T., Berrendero F., Ambrosino G., Cebeira M., Ramos J.A., Fernandez-Ruiz J.J., and Di Marzo V. Brain regional distribution of endocannabinoids: implications for their biosynthesis and biological function. Biochem Biophys Res Commun 256 (1999) 377-380
5. Bisogno T., Melck D., Bobrov M.Y., Gretskaya N.M., Bezuglov V.V., De Petrocellis L., and Di Marzo V. N-acyl-dopamines: novel synthetic CB(1) cannabinoid-receptor ligands and inhibitors of anandamide inactivation with cannabimimetic activity in vitro and in vivo. Biochem J 351 (2000) 817-824
6. Breder C.D., Dewitt D., and Kraig R.P. Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 355 (1995) 296-315
7. Canals S., Casarejos M.J., de Bernardo S., Rodriguez-Martin E., and Mena M.A. Nitric oxide triggers the toxicity due to glutathione depletion in midbrain cultures through 12-lipoxygenase. J Biol Chem 278 (2003) 21542-21549
8. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
9. Chandrasekharan N.V., Dai H., Roos K.L.T., Evanson N.K., Tomsik J., Elton T.S., and Simmons D.L. COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc Natl Acad Sci U S A 99 (2002) 13926-13931
10. Chu C.J., Huang S.M., De Petrocellis L., Bisogno T., Ewing S.A., Miller J.D., Zipkin R.E., Daddario N., Appendino G., Di Marzo V., and Walker J.M. N-oleoyldopamine, a novel endogenous capsaicin-like lipid that produces hyperalgesia. J Biol Chem 278 (2003) 13633-13639
11. Cortright D.N., Crandall M., Sanchez J.F., Zou T., Krause J.E., and White G. The tissue distribution and functional characterization of human VR1. Biochem Biophys Res Commun 281 (2001) 1183-1189
12. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., and Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384 (1996) 83-87
13. Cristino L., De Petrocellis L., Pryce G., Baker D., Guglielmotti V., and Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139 (2006) 1405-1415
14. De Petrocellis L., Bisogno T., Maccarrone M., Davis J.B., Finazzi-Agro A., and Di Marzo V. The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. J Biol Chem 276 (2001) 12856-12863
15. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., and Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 (1992) 1946-1949
16. Di Marzo V., Bisogno T., De Petrocellis L., Brandi I., Jefferson R.G., Winckler R.L., Davis J.B., Dasse O., Mahadevan A., Razdan R.K., and Martin B.R. Highly selective CB(1) cannabinoid receptor ligands and novel CB(1)/VR(1) vanilloid receptor "hybrid" ligands. Biochem Biophys Res Commun 281 (2001) 444-451
17. Di Marzo V., De Petrocellis L., Fezza F., Ligresti A., and Bisogno T. Anandamide receptors. Prostaglandins Leukot Essent Fatty Acids 66 (2002) 377-691
18. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J.-C., and Pomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372 (1994) 686-691
19. Di Marzo V., and Petrosino S. Endocannabinoids and the regulation of their levels in health and disease. Curr Opin Lipidol 18 (2007) 129-140
20. Egertova M., Cravatt B.F., and Elphick M.R. Comparative analysis of fatty acid amide hydrolase and cb(1) cannabinoid receptor expression in the mouse brain: evidence of a widespread role for fatty acid amide hydrolase in regulation of endocannabinoid signaling. Neuroscience 119 (2003) 481-496
21. Feinmark S.J., Begum R., Tsvetkov E., Goussakov I., Funk C.D., Siegelbaum S.A., and Bolshakov V.Y. 12-Lipoxygenase metabolites of arachidonic acid mediate metabotropic glutamate receptor-dependent long-term depression at hippocampal CA3-CA1 synapses. J Neurosci 23 (2003) 11427-11435
22. Gavva N.R., Klionsky L., Qu Y., Shi L., Tamir R., Edenson S., Zhang T.J., Viswanadhan V.N., Toth A., Pearce L.V., Vanderah T.W., Porreca F., Blumberg P.M., Lile J., Sun Y., Wild K., Louis J.C., and Treanor J.J. Molecular determinants of vanilloid sensitivity in TRPV1. J Biol Chem 279 (2004) 20283-20295
23. Gulyas A.I., Cravatt B.F., Bracey M.H., Dinh T.P., Piomelli D., Boscia F., and Freund T.F. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20 (2004) 441-448
24. Hillard C.J., Wilkison D.M., Edgemond W.S., and Campbell W.B. Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. Biochim Biophys Acta 1257 (1995) 249-256
25. Huang S.M., Bisogno T., Trevisani M., Al-Hayani A., De Petrocellis L., Fezza F., Tognetto M., Petros T.J., Krey J.F., Chu C.J., Miller J.D., Davies S.N., Geppetti P., Walker J.M., and Di Marzo V. An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc Natl Acad Sci U S A 99 (2002) 8400-8405
26. Iversen L., and Chapman V. Cannabinoids: a real prospect for pain relief?. Curr Opin Pharmacol 2 (2002) 50-55
27. Jordt S.E., and Julius D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108 (2002) 421-430
28. Kaplan G.P., Hartman B.K., and Creveling C.R. Immunohistochemical demonstration of catechol-o-methyltransferase in mammalian brain. Brain Res 167 (1979) 241-250
29. Karhunen T., Tilgmann C., Ulmanen I., and Panula P. Catechol-O-methyltransferase (COMT) in rat brain: immunoelectron microscopic study with an antiserum against rat recombinant COMT protein. Neurosci Lett 18 (1995) 57-60
30. Kaufmann W.E., Worley P.F., Pegg J., Bremer M., and Isakson P. COX-2, a synaptically induced enzyme, is expressed by excitatory neurons at postsynaptic sites in rat cerebral cortex. Proc Natl Acad Sci U S A 93 (1996) 2317-2321
31. Kim J., and Alger B.E. Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nat Neurosci 7 (2004) 697-698
32. Kofalvi A., Oliveira C.R., and Cunha R.A. Lack of evidence for functional TRPV1 vanilloid receptors in rat hippocampal nerve terminals. Neurosci Lett 403 (2006) 151-156
33. Kozak K.R., Prusakiewicz J.L., and Marnett L.J. Oxidative metabolism of endocannabinoids by COX-2. Curr Pharm Des 10 (2004) 659-667
34. Leung D., Saghatelian A., Simon G.M., and Cravatt B.F. Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 45 (2006) 4720-4726
35. Liapi A., and Wood J.N. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur J Neurosci 22 (2005) 825-834
36. Liu J., Wang L., Harvey-White J., Osei-Hyiaman D., Razdan R., Gong Q., Chan A.C., Zhou Z., Huang B.X., Kim H.Y., and Kunos G. A biosynthetic pathway for anandamide. Proc Natl Acad Sci U S A 103 (2006) 13345-133450
37. Maccarrone M., van der Stelt M., Rossi A., Veldink G.A., Vliegenthart J.F., and Agrò A.F. Anandamide hydrolysis by human cells in culture and brain. J Biol Chem 273 (1998) 32332-32339
38. Maccarrone M., Salvati S., Bari M., and Finazzi-Agro A. Anandamide and 2-arachidonoylglycerol inhibit fatty acid amide hydrolase by activating the lipoxygenase pathway of the arachidonate cascade. Biochem Biophys Res Commun 278 (2000) 576-583
39. Maione S., Bisogno T., de Novellis V., Palazzo E., Cristino L., Valenti M., Petrosino S., Guglielmotti V., Rossi F., and Di Marzo V. 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 (2006) 969-982
40. Marinelli S., Di Marzo V., Florenzano F., Fezza F., Viscomi M.T., van der Stelt M., Bernardi G., Molinari M., Maccarrone M., and Mercuri N.B. N-arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32 (2007) 298-308
41. Marsch R., Foeller E., Rammes G., Bunck M., Kossl M., Holsboer F., Zieglgansberger W., Landgraf R., Lutz B., and Wotjak C.T. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27 (2007) 832-839
42. Matias I., Chen J., De Petrocellis L., Bisogno T., Ligresti A., Fezza F., Krauss A.H., Shi L., Protzman C.E., Li C., Liang Y., Nieves A.L., Kedzie K.M., Burk R.M., Di Marzo V., and Woodward D.F. Prostaglandin ethanolamides (prostamides): in vitro pharmacology and metabolism. J Pharmacol Exp Ther 309 (2004) 745-757
43. Matsumoto M., Weickert C.S., Beltaifa S., Kolachana B., Chen J., Hyde T.M., Herman M.M., Weinberger D.R., and Kleinman J.E. Catechol O-methyltransferase (COMT) mRNA expression in the dorsolateral prefrontal cortex of patients with schizophrenia. Neuropsychopharmacology 28 (2003) 1521-1530
44. Mezey E., Tóth Z.E., Cotright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., and Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci U S A 97 (2000) 3655-3660
45. Morishita J., Okamoto Y., Tsuboi K., Ueno M., Sakamoto H., Maekawa N., and Ueda N. Regional distribution and age-dependent expression of N-acylphosphatidylethanolamine-hydrolyzing phospholipase D in rat brain. J Neurochem 94 (2005) 753-762
46. Movahed P., Jonsson B.A., Birnir B., Wingstrand J.A., Jorgensen T.D., Ermund A., Sterner O., Zygmunt P.M., and Hogestatt E.D. Endogenous unsaturated C18 N-acylethanolamines are vanilloid receptor (TRPV1) agonists. J Biol Chem 280 (2005) 38496-38504
47. Nishiyama M., Watanabe T., Ueda N., Tsukamoto H., and Watanabe K. Arachidonate 12-lipoxygenase is localized in neurons, glial cells, and endothelial cells of the canine brain. J Histochem Cytochem 41 (1993) 111-117
48. Okamoto Y., Morishita J., Tsuboi K., Tonai T., and Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279 (2004) 5298-5305
49. Price T.J., Patwardhan A., Akopian A.N., Hargreaves K.M., and Flores C.M. Modulation of trigeminal sensory neuron activity by the dual cannabinoid-vanilloid agonists anandamide, N-arachidonoyl-dopamine and arachidonyl-2-chloroethylamide. Br J Pharmacol 141 (2004) 1118-1130
50. Rice A.S., Farquhar-Smith W.P., and Nagy I. Endocannabinoids and pain: spinal and peripheral analgesia in inflammation and neuropathy. Prostaglandins Leukot Essent Fatty Acids 66 (2002) 243-256
51. Roberts J.C., Davis J.B., and Benham C.D. [H3]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res 995 (2004) 176-183
52. Sanchez J.F., Krause J.E., and Cortright D.N. The distribution and regulation of vanilloid receptor VR1 and VR1 5′ splice variant RNA expression in rat. Neuroscience 107 (2001) 373-381
53. Slanina K.A., Roberto M., and Schweitzer P. Endocannabinoids restrict hippocampal long-term potentiation via CB1. Neuropharmacology 49 (2005) 660-668
54. Slanina K.A., and Schweitzer P. Inhibition of cyclooxygenase-2 elicits a CB1-mediated decrease of excitatory transmission in rat CA1 hippocampus. Neuropharmacology 49 (2005) 653-659
55. Smart D., Gunthorpe M.J., Jerman J.C., Nasir S., Gray J., Muir A.I., Chambers J.K., Randall A.D., and Davis J.B. The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br J Pharmacol 129 (2000) 227-230
56. Starowicz K., Nigam S., and Di Marzo V. Biochemistry and pharmacology of endovanilloids. Pharmacol Ther 114 (2007) 13-33
57. Szabo T., Biro T., Gonzalez A.F., Palkovits M., and Blumberg P.M. Pharmacological characterization of vanilloid receptor located in the brain. Brain Res Mol Brain Res 98 (2002) 51-57
58. Szallasi A., and Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol Rev 51 (1999) 159-211
59. Szallasi A., and Di Marzo V. New perspectives on enigmatic vanilloid receptors. Trends Neurosci 23 (2000) 491-497
60. Tóth A., Boczan J., Kedei N., Lizanecz E., Bagi Z., Papp Z., Edes I., Csiba L., and Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135 (2005) 162-168
61. Tsou K., Brown S., Sañudo-Peña M.C., Mackie K., and Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 (1998) 393-411
62. Ueda N., Kurahashi Y., Yamamoto S., and Tokunaga T. Partial purification and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide. J Biol Chem 270 (1995) 23823-23827
63. Uz T., Pesold C., Longone P., and Manev H. Aging-associated up-regulation of neuronal 5-lipoxygenase expression: putative role in neuronal vulnerability. FASEB J 12 (1998) 439-449
64. van der Stelt M., and Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 271 (2004) 1827-1834
65. 2+ influx via TRPV1 channels. EMBO J 24 (2005) 3026-3037
66. Vane J.R., Bakhle Y.S., and Botting R.M. Cyclooxygenase 1 and 2. Annu Rev Pharmacol Toxicol 38 (1998) 97-120
67. Walker J.M., and Huang S.M. Endocannabinoids in pain modulation. Prostaglandins Leukot Essent Fatty Acids 66 (2002) 235-242
68. Woodward D.F., Liang Y., and Krauss A.H. Prostamides (prostaglandin-ethanolamides) and their pharmacology. Br J Pharmacol (2007) 2007 Aug 27; [Epub ahead of print] doi: 10.1038/sj.bjp.0707434
69. Yu M., Ives D., and Ramesha C.S. Synthesis of prostaglandin E2 ethanolamide from anandamide by cyclooxygenase-2. J Biol Chem 272 (1997) 21181-21186
70. Zygmunt P.M., Peterson J., Anderson D.A., Chuang H., Sorgard M., Di Marzo V., Julius D., and Hogestatt E.D. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400 (1999) 452-457