Cannabinoid receptor agonists potentiate action potential-independent release of GABA in the dentate gyrus through a CB1 receptor-independent mechanism

Journal of Physiology

Volumn 589, Issue 15, 2011, Pages 3801-3821

  Hofmann, Mackenzie E ^a,b   Bhatia, Chinki ^a   Frazier, Charles J ^a,b  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 ARACHIDONOYLGLYCEROL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 AMINOBUTYRIC ACID; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ANANDAMIDE; CALCIUM; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CAPSAZEPINE; FORSKOLIN; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; SURAMIN; VANILLOID RECEPTOR 1;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHELATION; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVATION; EVOKED CORTICAL RESPONSE; EXOCYTOSIS; FACILITATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTRACELLULAR RECORDING; MALE; MEMORY; MOSSY FIBER; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; ARACHIDONIC ACIDS; BENZOXAZINES; CALCIUM; CANNABINOIDS; EXOCYTOSIS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GLYCERIDES; MALE; MORPHOLINES; MOSSY FIBERS, HIPPOCAMPAL; NAPHTHALENES; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; SYNAPTIC TRANSMISSION;

EID: 79960805530     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.211482     Document Type: Article

References (89)

1. Al-Hayani A & Davies SN (2002). Effect of cannabinoids on synaptic transmission in the rat hippocampal slice is temperature-dependent. Eur J Pharmacol 442, 47-54.
2. Bajo M, Roberto M & Schweitzer P (2009). Differential alteration of hippocampal excitatory synaptic transmission by cannabinoid ligands. J Neurosci Res 87, 766-775.
3. Beindl W, Mitterauer T, Hohenegger M, Ijzerman AP, Nanoff C & Freissmuth M (1996). Inhibition of receptor/G protein coupling by suramin analogues. Mol Pharmacol 50, 415-423.
4. Blair RE, Deshpande LS, Sombati S, Falenski KW, Martin BR & Delorenzo RJ (2006). Activation of the cannabinoid type-1 receptor mediates the anticonvulsant properties of cannabinoids in the hippocampal neuronal culture models of acquired epilepsy and status epilepticus. J Pharmacol Exp Ther 317, 1072-1078.
5. Bodor AL, Katona I, Nyiri G, Mackie K, Ledent C, Hajos N & Freund TF (2005). Endocannabinoid signalling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 25, 6845-6856.
6. Bojanowski K, Lelievre S, Markovits J, Couprie J, Jacquemin-Sablon A & Larsen AK (1992). Suramin is an inhibitor of DNA topoisomerase II in vitro and in Chinese hamster fibrosarcoma cells. Proc Natl Acad Sci U S A 89, 3025-3029.
7. Braga MFM, Pereira EFR, Marchioro M & Albuquerque EX (1999). Lead increases tetrodotoxin-insensitive spontaneous release of glutamate and GABA from hippocampal neurons. Brain Res 826, 10-21.
8. Breivogel CS, Griffin G, Di Marzo V & Martin BR (2001). Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Mol Pharmacol 60, 155-163.
9. Bruno MJ, Koeppe RE 2nd & Andersen OS (2007). Docosahexaenoic acid alters bilayer elastic properties. Proc Natl Acad Sci U S A 104, 9638-9643.
10. Bultmann R, Wittenburg H, Pause B, Kurz G, Nickel P & Starke K (1996). P2-purinoceptor antagonists: III. Blockade of P2-purinoceptor subtypes and ecto-nucleotidases by compounds related to suramin. Naunyn Schmiedebergs Arch Pharmacol 354, 498-504.
11. Carter AG & Regehr WG (2002). Quantal events shape cerebellar interneuron firing. Nat Neurosci 5, 1309-1318.
12. Chevaleyre V, Takahashi KA & Castillo PE (2006). Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29, 37-76.
13. Chung WC & Kermode JC (2005). Suramin disrupts receptor-G protein coupling by blocking association of G protein α and βγ subunits. J Pharmacol Exp Ther 313, 191-198.
14. Cibulsky SM & Sather WA (1999). Block by ruthenium red of cloned neuronal voltage-gated calcium channels. J Pharmacol Exp Ther 289, 1447-1453.
15. Di Marzo V (2006). Non-CB1 non-CB2 receptors for endocannabinoids. In Endocannabinoids: The Brain and Body's Marijuana and Beyond, ed. Onaivi ES, Sugiura T & Di Marzo V, pp. 151-174. Taylor and Francis, Boca Raton.
16. 2 receptor-mediated actions of anandamide in mouse brain. J Neurochem 75, 2434-2444.
17. Di Marzo V, De PL, Fezza F, Ligresti A & Bisogno T (2002). Anandamide receptors. Prostaglandins Leukot Essent Fatty Acids 66, 377-391.
18. Diana MA & Marty A (2004). Endocannabinoid-mediated short-term synaptic plasticity: depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). Br J Pharmacol 142, 9-19.
19. Domenici MR, Azad SC, Marsicano G, Schierloh A, Wotjak CT, Dodt HU, Zieglgansberger W, Lutz B & Rammes G (2006). Cannabinoid receptor type 1 located on presynaptic terminals of principal neurons in the forebrain controls glutamatergic synaptic transmission. J Neurosci 26, 5794-5799.
20. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
21. Frazier CJ, Strowbridge BW & Papke RL (2003). Nicotinic receptors on local circuit neurons in dentate gyrus: a potential role in regulation of granule cell excitability. J Neurophysiol 89, 3018-3028.
22. Freissmuth M, Boehm S, Beindl W, Nickel P, Ijzerman AP, Hohenegger M & Nanoff C (1996). Suramin analogues as subtype-selective G protein inhibitors. Mol Pharmacol 49, 602-611.
23. Freund TF, Katona I & Piomelli D (2003). Role of endogenous cannabinoids in synaptic signalling. Physiol Rev 83, 1017-1066.
24. Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA & Doherty P (2010). Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice The Journal of Neuroscience 30, 2017-2024.
25. 2+- how spontaneous is spontaneous neurotransmitter release? Cell Calcium 43, 9-15.
26. Groemer TW & Klingauf J (2007). Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nat Neurosci 10, 145-147.
27. Hillard CJ (2000). Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostaglandins Other Lipid Mediat 61, 3-18.
28. Hofmann ME, Nahir B & Frazier CJ (2006). Endocannabinoid-mediated depolarization-induced suppression of inhibition in hilar mossy cells of the rat dentate gyrus. J Neurophysiol 96, 2501-2512.
29. Hofmann ME, Nahir B & Frazier CJ (2008). Excitatory afferents to CA3 pyramidal cells display differential sensitivity to CB1 dependent inhibition of synaptic transmission. Neuropharmacology 55, 1140-1146.
30. Howard AL, Neu A, Morgan RJ, Echegoyen JC & Soltesz I (2007). Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: evidence for single-cell homeostasis in a hyperexcitable network. J Neurophysiol 97, 2394-2409.
31. Jarvis MF & Khakh BS (2009). ATP-gated P2X cation-channels. Neuropharmacology 56, 208-215.
32. Katona I, Urban GM, Wallace M, Ledent C, Jung KM, Piomelli D, Mackie K & Freund TF (2006). Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26, 5628-5637.
33. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, Watanabe M, Ohno-Shosaku T & Kano M (2006). The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26, 2991-3001.
34. Kerr AM & Capogna M (2007). Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus. J Physiol 578, 451-470.
35. Kiss T (2005). G-protein coupled activation of potassium channels by endogenous neuropeptides in snail neurons. Eur J Neurosci 21, 2177-2185.
36. Klinger M, Freissmuth M, Nickel P, Stabler-Schwarzbart M, Kassack M, Suko J & Hohenegger M (1999). Suramin and suramin analogs activate skeletal muscle ryanodine receptor via a calmodulin binding site. Mol Pharmacol 55, 462-472.
37. Kreitzer FR & Stella N (2009). The therapeutic potential of novel cannabinoid receptors. Pharmacol Ther 122, 83-96.
38. Kuster JE, Stevenson JI, Ward SJ, D'Ambra TE & Haycock DA (1993). Aminoalkylindole binding in rat cerebellum: selective displacement by natural and synthetic cannabinoids. J Pharmacol Exp Ther 264, 1352-1363.
39. Lauckner JE, Jensen JB, Chen HY, Lu HC, Hille B & Mackie K (2008). GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci U S A 105, 2699-2704.
40. Lehmann N, Krishna Aradhyam G & Fahmy K (2002). Suramin affects coupling of rhodopsin to transducin. Biophys J 82, 793-802.
41. Li YX, Zhang Y, Lester HA, Schuman EM & Davidson N (1998). Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J Neurosci 18, 10231-10240.
42. Lindsly C & Frazier CJ (2010). Two distinct and activity-dependent mechanisms contribute to autoreceptor-mediated inhibition of GABAergic afferents to hilar mossy cells. J Physiol 588, 2801-2822.
43. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP & Marty A (2000). Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3, 1256-1265.
44. Lu T & Trussell LO (2000). Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26, 683-694.
45. Lundbaek JA (2008). Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs. J Gen Physiol 131, 421-429.
46. Lundbaek JA, Birn P, Hansen AJ, Sogaard R, Nielsen C, Girshman J, Bruno MJ, Tape SE, Egebjerg J, Greathouse DV, Mattice GL, Koeppe RE 2nd & Andersen OS (2004). Regulation of sodium channel function by bilayer elasticity: the importance of hydrophobic coupling. Effects of micelle-forming amphiphiles and cholesterol. J Gen Physiol 123, 599-621.
47. Lundbaek JA, Birn P, Tape SE, Toombes GE, Sogaard R, Koeppe RE 2nd, Gruner SM, Hansen AJ & Andersen OS (2005). Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. Mol Pharmacol 68, 680-689.
48. Mackie K (2008). Signalling via CNS cannabinoid receptors. Mol Cell Endocrinol 286, S60-S65.
49. + channel TASK-1. EMBO J 20, 47-54.
50. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, Van Der Stelt 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.
51. McKinney RA, Capogna M, Durr R, Gahwiler BH & Thompson SM (1999). Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2, 44-49.
52. McLaren GJ, Kennedy C & Sneddon P (1995). The effects of suramin on purinergic and noradrenergic neurotransmission in the rat isolated tail artery. Eur J Pharmacol 277, 57-61.
53. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgansberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G & Lutz B (2006). The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51, 455-466.
54. Nahir B, Bhatia C & Frazier CJ (2007). Presynaptic inhibition of excitatory afferents to hilar mossy cells. J Neurophysiol 97, 4036-4047.
55. Navarrete M & Araque A (2008). Endocannabinoids mediate neuron-astrocyte communication. Neuron 57, 883-893.
56. 1 receptor-dependent and -independent inhibition of excitatory postsynaptic currents in the hippocampus by WIN 55, 212-2. Neuropharmacology 54, 51-57.
57. Nyilas R, Dudok B, Urban GM, Mackie K, Watanabe M, Cravatt BF, Freund TF & Katona I (2008). Enzymatic machinery for endocannabinoid biosynthesis associated with calcium stores in glutamatergic axon terminals. J Neurosci 28, 1058-1063.
58. Ohno-Shosaku T, Maejima T & Kano M (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729-738.
59. Oz M (2006a). Receptor-independent actions of cannabinoids on cell membranes: focus on endocannabinoids. Pharmacol Ther 111, 114-144.
60. Oz M (2006b). Receptor-independent effects of endocannabinoids on ion channels. Curr Pharm Des 12, 227-239.
61. Papineni RVL (2002). Suramin interacts with the calmodulin binding site on the ryanodine receptor, RYR1. J Biol Chem 277, 49167-49174.
62. Popescu IR, Morton LA, Franco A, Di S, Ueta Y & Tasker JG (2010). Synchronized bursts of miniature inhibitory postsynaptic currents. J Physiol 588, 939-951.
63. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson NO, Leonova J, Elebring T, Nilsson K, Drmota T & Greasley PJ (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152, 1092-1101.
64. Saitoe M, Schwarz TL, Umbach JA, Gundersen CB & Kidokoro Y (2001). Absence of junctional glutamate receptor clusters in Drosophila mutants lacking spontaneous transmitter release. Science 293, 514-517.
65. Sang N, Zhang J & Chen C (2010). Anandamide potentiation of miniature spontaneous excitatory synaptic transmission is mediated via IP3 pathway. Neurochem Int 56, 590-596.
66. Sara Y, Virmani T, Deak F, Liu X & Kavalali ET (2005). An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563-573.
67. Sciancalepore M, Savic N, Gyori J & Cherubini E (1998). Facilitation of miniature GABAergic currents by ruthenium red in neonatal rat hippocampal neurons. J Neurophysiol 80, 2316-2322.
68. Sharma G & Vijayaraghavan S (2003). Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38, 929-939.
69. Shen M & Thayer SA (1998). The cannabinoid agonist Win55, 212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Research 783, 77-84.
70. A receptor function is regulated by lipid bilayer elasticity. Biochemistry 45, 13118-13129.
71. Sugiura T, Kishimoto S, Oka S & Gokoh M (2006). Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog Lipid Res 45, 405-446.
72. Sugiura T, Kobayashi Y, Oka S & Waku K (2002). Biosynthesis and degradation of anandamide and 2-arachidonoylglycerol and their possible physiological significance. Prostaglandins Leukot Essent Fatty Acids 66, 173-192.
73. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682.
74. Takahashi KA & Castillo PE (2006). The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus. Neuroscience 139, 795-802.
75. Talley EM, Solorzano G, Lei Q, Kim D & Bayliss DA (2001). CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21, 7491-7505.
76. Tanimura A, Yamazaki M, Hashimotodani Y, Uchigashima M, Kawata S, Abe M, Kita Y, Hashimoto K, Shimizu T, Watanabe M, Sakimura K & Kano M (2010). The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase α mediates retrograde suppression of synaptic transmission. Neuron 65, 320-327.
77. Taverna S, Tkatch T, Metz AE & Martina M (2005). Differential expression of TASK channels between horizontal interneurons and pyramidal cells of rat hippocampus. J Neurosci 25, 9162-9170.
78. Tigyi G & Parrill AL (2003). Molecular mechanisms of lysophosphatidic acid action. Prog Lipid Res 42, 498-526.
79. Torborg CL, Berg AP, Jeffries BW, Bayliss DA & McBain CJ (2006). TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations. J Neurosci 26, 7362-7367.
80. Trettel J & Levine ES (2003). Endocannabinoids mediate rapid retrograde signalling at interneuron right-arrow pyramidal neuron synapses of the neocortex. J Neurophysiol 89, 2334-2338.
81. Trudeau LE, Doyle RT, Emery DG & Haydon PG (1996a). Calcium-independent activation of the secretory apparatus by ruthenium red in hippocampal neurons: a new tool to assess modulation of presynaptic function. J Neurosci 16, 46-54.
82. Trudeau LE, Emery DG & Haydon PG (1996b). Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 17, 789-797.
83. Vida I & Frotscher M (2000). A hippocampal interneuron associated with the mossy fibre system. Proc Natl Acad Sci U S A 97, 1275-1280.
84. Wang YF & Hatton GI (2007). Dominant role of betagamma subunits of G-proteins in oxytocin-evoked burst firing. J Neurosci 27, 1902-1912.
85. Wasser CR & Kavalali ET (2008). Leaky synapses: Regulation of spontaneous neurotransmission in central synapses. Neuroscience 158, 177-188.
86. Wilson RI & Nicoll RA (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
87. 2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar purkinje cells. J Neurosci 26, 86-95.
88. Yokoyama K, Baker DL, Virag T, Liliom K, Byun HS, Tigyi G & Bittman R (2002). Stereochemical properties of lysophosphatidic acid receptor activation and metabolism. Biochim Biophys Acta 1582, 295-308.
89. Zhu PJ & Lovinger DM (2005). Retrograde endocannabinoid signalling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J Neurosci 25, 6199-6207.