Identification of mRNA for endocannabinoid biosynthetic enzymes within hippocampal pyramidal cells and CA1 stratum radiatum interneuron subtypes using quantitative real-time polymerase chain reaction

Neuroscience

Volumn 218, Issue , 2012, Pages 89-99

  Merrill, C B ^a   McNeil, M ^a   Williamson, R C ^a   Poole, B R ^a   Nelson, B ^a   Sudweeks, S ^a   Edwards, J G ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Calbindin; Calretinin; CCK; Eicosanoid; LTD; MGluR

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; DIACYLGLYCEROL LIPASE ALPHA; ENDOCANNABINOID BIOSYNTHETIC ENZYME; ENZYME; LIPOPROTEIN LIPASE; MESSENGER RNA; METABOTROPIC RECEPTOR 1; N ACYL PHOSPHATIDYLETHANOL AMINE SPECIFIC PHOSPHOLIPASE D; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; INTERNEURON; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REAL TIME QUANTITATIVE POLYMERASE CHAIN REACTION; STRATUM RADIATUM;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; ENDOCANNABINOIDS; INTERNEURONS; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84863780403     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.05.012     Document Type: Article

References (66)

1. Abush H., Akirav I. Cannabinoids modulate hippocampal memory and plasticity. Hippocampus 2010, 20:1126-1138.
2. Alger B.E. Endocannabinoids at the synapse a decade after the Dies Mirabilis (29 March 2001): what we still do not know. J Physiol 2012, 590:2203-2212.
3. Alger B.E., Pitler T.A. Retrograde signaling at GABAA-receptor synapses in the mammalian CNS. Trends Neurosci 1995, 18:333-340.
4. Ascoli G.A., Alonso-Nanclares L., Anderson S.A., Barrionuevo G., Benavides-Piccione R., Burkhalter A., Buzsaki G., Cauli B., Defelipe J., Fairen A., Feldmeyer D., Fishell G., Fregnac Y., Freund T.F., Gardner D., Gardner E.P., Goldberg J.H., Helmstaedter M., Hestrin S., Karube F., Kisvarday Z.F., Lambolez B., Lewis D.A., Marin O., Markram H., Munoz A., Packer A., Petersen C.C., Rockland K.S., Rossier J., Rudy B., Somogyi P., Staiger J.F., Tamas G., Thomson A.M., Toledo-Rodriguez M., Wang Y., West D.C., Yuste R. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 2008, 9:557-568.
5. Bacci A., Huguenard J.R., Prince D.A. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 2004, 431:312-316.
6. Beierlein M., Regehr W.G. Local interneurons regulate synaptic strength by retrograde release of endocannabinoids. J Neurosci 2006, 26:9935-9943.
7. Bennion D., Jensen T., Walther C., Hamblin J., Wallmann A., Couch J., Blickenstaff J., Castle M., Dean L., Beckstead S., Merrill C., Muir C., St Pierre T., Williams B., Daniel S., Edwards J.G. Transient receptor potential vanilloid 1 agonists modulate hippocampal CA1 LTP via the GABAergic system. Neuropharmacology 2011, 61:730-738.
8. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 1973, 232:331-356.
9. Boscia F., Ferraguti F., Moroni F., Annunziato L., Pellegrini-Giampietro D.E. MGlu1α receptors are co-expressed with CB1 receptors in a subset of interneurons in the CA1 region of organotypic hippocampal slice cultures and adult rat brain. Neuropharmacology 2008, 55:428-439.
10. Buhl E.H., Szilagyi T., Halasy K., Somogyi P. Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro. Hippocampus 1996, 6:294-305.
11. Caterina M., Schumacher M., Tominaga M., Rosen T., Levine J., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
12. Cavanaugh D.J., Chesler A.T., Jackson A.C., Sigal Y.M., Yamanaka H., Grant R., O'Donnell D., Nicoll R.A., Shah N.M., Julius D., Basbaum A.I. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J Neurosci 2011, 31:5067-5077.
13. Chavez A.E., Chiu C.Q., Castillo P.E. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 2010, 13:1511-1518.
14. Chuang S.C., Zhao W., Young S.R., Conquet F., Bianchi R., Wong R.K. Activation of group I mGluRs elicits different responses in murine CA1 and CA3 pyramidal cells. J Physiol 2002, 541:113-121.
15. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 2006, 139:1405-1415.
16. Cristino L., Starowicz K., De Petrocellis L., Morishita J., Ueda N., Guglielmotti V., Di Marzo V. Immunohistochemical localization of anabolic and catabolic enzymes for anandamide and other putative endovanilloids in the hippocampus and cerebellar cortex of the mouse brain. Neuroscience 2008, 151:955-968.
17. De Petrocellis L., Di Marzo V. Lipids as regulators of the activity of transient receptor potential type V1 (TRPV1) channels. Life Sci 2005, 77:1651-1666.
18. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J.-C., Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 1994, 372:686-691.
19. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 1992, 89:4363-4367.
20. Edwards D.A., Kim J., Alger B.E. Multiple mechanisms of endocannabinoid response initiation in hippocampus. J Neurophysiol 2006, 95:67-75.
21. Egertová M., Simon G.M., Cravatt B.F., Elphick M.R. 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 2008, 506:604-615.
22. Feinmark S.J., Begum R., Tsvetkov E., Goussakov I., Funk C.D., Siegelbaum S.A., Bolshakov V.Y. 12-Lipoxygenase metabolites of arachidonic acid mediate metabotropic glutamate receptor-dependent long-term depression at hippocampal CA3-CA1 synapses. J Neurosci 2003, 23:11427-11435.
23. Ferraguti F., Cobden P., Pollard M., Cope D., Shigemoto R., Watanabe M., Somogyi P. Immunolocalization of metabotropic glutamate receptor 1alpha (mGluR1alpha) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus 2004, 14:193-215.
24. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
25. Fuentealba P., Begum R., Capogna M., Jinno S., Márton L.F., Csicsvari J., Thomson A., Somogyi P., Klausberger T. Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 2008, 57:917-929.
26. Galarreta M., Erdelyi F., Szabo G., Hestrin S. Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 2004, 24:9770-9778.
27. Gee C.E., Benquet P., Gerber U. Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol 2003, 546:655-664.
28. Gibson H.E., Edwards J.G., Page R.S., Van Hook M.J., Kauer J.A. TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 2008, 57:746-759.
29. Gulyas A.I., Hajos N., Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 1996, 16:3397-3411.
30. Heifets B.D., Castillo P.E. Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 2009, 71:283-306.
31. Hill E.L., Gallopin T., Ferezou I., Cauli B., Rossier J., Schweitzer P., Lambolez B. Functional CB1 receptors are broadly expressed in neocortical GABAergic and glutamatergic neurons. J Neurophysiol 2007, 97:2580-2589.
32. Hoffman A.F., Riegel A.C., Lupica C.R. Functional localization of cannabinoid receptors and endogenous cannabinoid production in distinct neuron populations of the hippocampus. Eur J Neurosci 2003, 18:524-534.
33. Holderith N., Nemeth B., Papp O.I., Veres J.M., Nagy G.A., Hajos N. Cannabinoids attenuate hippocampal gamma oscillations by suppressing excitatory synaptic input onto CA3 pyramidal neurons and fast spiking basket cells. J Physiol 2011, 589:4921-4934.
34. Huber K.M., Roder J.C., Bear M.F. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J Neurophysiol 2001, 86:321-325.
35. Hwang S.W., Cho H., Kwak J., Lee S.Y., Kang C.J., Jung J., Cho S., Min K.H., Suh Y.G., Kim D., Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci U S A 2000, 97:6155-6160.
36. Jinno S., Kosaka T. Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 2002, 449:1-25.
37. Jinno S., Kosaka T. Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci Res 2006, 56:229-245.
38. Katona I., Sperlagh B., Sik A., Kafalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999, 19:4544-4558.
39. Katona I., Urban G.M., Wallace M., Ledent C., Jung K.M., Piomelli D., Mackie K., Freund T.F. Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 2006, 26:5628-5637.
40. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 1995, 18:527-535.
41. Kerner J.A., Standaert D.G., Penney J.B., Young A.B., Landwehrmeyer G.B. Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Mol Brain Res 1997, 48:259-269.
42. Klausberger T. GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 2009, 30:947-957.
43. Kofalvi A., Oliveira C., Cunha R. Lack of evidence for functional TRPV(1) vanilloid receptors in rat hippocampal nerve terminals. Neurosci Lett 2006, 403:151-156.
44. Le Duigou C., Holden T., Kullmann D.M. Short- and long-term depression at glutamatergic synapses on hippocampal interneurons by group I mGluR activation. Neuropharmacology 2011, 60:748-756.
45. 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., Kunos G. A biosynthetic pathway for anandamide. Proc Natl Acad Sci U S A 2006, 103:13345-13350.
46. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25:402-408.
47. Ludanyi A., Hu S.S., Yamazaki M., Tanimura A., Piomelli D., Watanabe M., Kano M., Sakimura K., Magloczky Z., Mackie K., Freund T.F., Katona I. Complementary synaptic distribution of enzymes responsible for synthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in the human hippocampus. Neuroscience 2011, 174:50-63.
48. Lujan R., Nusser Z., Roberts J.D., Shigemoto R., Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 1996, 8:1488-1500.
49. Marsicano G., Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 1999, 11:4213-4225.
50. Morishita J., Okamoto Y., Tsuboi K., Ueno M., Sakamoto H., Maekawa N., Ueda N. Regional distribution and age-dependent expression of N-acylphosphatidylethanolamine-hydrolyzing phospholipase D in rat brain. J Neurochem 2005, 94:753-762.
51. Nishiyama M., Watanabe T., Ueda N., Tsukamoto H., Watanabe K. Arachidonate 12-lipoxygenase is localized in neurons, glial cells, and endothelial cells of the canine brain. J Histochem Cytochem 1993, 41:111-117.
52. Oudin M.J., Hobbs C., Doherty P. DAGL-dependent endocannabinoid signalling: roles in axonal pathfinding, synaptic plasticity and adult neurogenesis. Eur J Neurosci 2011, 34:1634-1646.
53. Pawelzik H., Bannister A.P., Deuchars J., Ilia M., Thomson A.M. Modulation of bistratified cell IPSPs and basket cell IPSPs by pentobarbitone sodium, diazepam and Zn2+: dual recordings in slices of adult rat hippocampus. Eur J Neurosci 1999, 11:3552-3564.
54. Placzek E.A., Okamoto Y., Ueda N., Barker E.L. Mechanisms for recycling and biosynthesis of endogenous cannabinoids anandamide and 2-arachidonylglycerol. J Neurochem 2008, 107:987-1000.
55. Romano C., Sesma M.A., McDonald C.T., O'Malley K., Van den Pol A.N., Olney J.W. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol 1995, 355:455-469.
56. Sanchez J., Krause J., Cortright D. The distribution and regulation of vanilloid receptor VR1 and VR1 5' splice variant RNA expression in rat. Neuroscience 2001, 107:373-381.
57. Shigemoto R., Kinoshita A., Wada E., Nomura S., Ohishi H., Takada M., Flor P.J., Neki A., Abe T., Nakanishi S., Mizuno N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 1997, 17:7503-7522.
58. Simon G.M., Cravatt B.F. Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo. Mol Biosyst 2010, 6:1411-1418.
59. Smart D., Gunthorpe M.J., Jerman J.C., Nasir S., Gray J., Muir A.I., Chambers J.K., Randall A.D., Davis J.B. The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br J Pharmacol 2000, 129:227-230.
60. Szilagyi T., Orban-Kis K., Horvath E., Metz J., Pap Z., Pavai Z. Morphological identification of neuron types in the rat hippocampus. Rom J Morphol Embryol 2011, 52:15-20.
61. Tanimura A., Yamazaki M., Hashimotodani Y., Uchigashima M., Kawata S., Abe M., Kita Y., Hashimoto K., Shimizu T., Watanabe M., Sakimura K., Kano M. The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase α mediates retrograde suppression of synaptic transmission. Neuron 2010, 65:320-327.
62. Tóth A., Boczán J., Kedei N., Lizanecz E., Bagi Z., Papp Z., édes I., Csiba L., Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Mol Brain Res 2005, 135:162-168.
63. Ueda N., Okamoto Y., Morishita J. N-acylphosphatidylethanolamine-hydrolyzing phospholipase D: A novel enzyme of the β-lactamase fold family releasing anandamide and other N-acylethanolamines. Life Sci 2005, 77:1750-1758.
64. van Hooft J.A., Giuffrida R., Blatow M., Monyer H. Differential expression of group I metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J Neurosci 2000, 20:3544-3551.
65. Wierenga C.J., Mullner F.E., Rinke I., Keck T., Stein V., Bonhoeffer T. Molecular and electrophysiological characterization of GFP-expressing CA1 interneurons in GAD65-GFP mice. PLoS One 2010, 5:e15915.
66. Wittner L., Henze D.A., Zaborszky L., Buzsaki G. Hippocampal CA3 pyramidal cells selectively innervate aspiny interneurons. Eur J Neurosci 2006, 24:1286-1298.