Presynaptic long-term depression mediated by Gi/o-coupled receptors

Trends in Neurosciences

Volumn 37, Issue 11, 2014, Pages 663-673

  Atwood, Brady K ^a   Lovinger, David M ^a   Mathur, Brian N ^b  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Gi o GPCR; Long term synaptic plasticity; Neurotransmitter release; Plasticity mechanisms; Presynaptic plasticity; Synaptic inhibition; Vesicle release machinery

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; METABOTROPIC RECEPTOR;

LONG TERM DEPRESSION; MOLECULAR BIOLOGY; NERVE CELL PLASTICITY; NERVE ENDING; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; DEPRESSION; HUMAN; LONG TERM POTENTIATION; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; DEPRESSION; HUMANS; LONG-TERM POTENTIATION; NEURONAL PLASTICITY; NEURONS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION;

EID: 84910067651     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2014.07.010     Document Type: Review

References (120)

1. Yoon B.J., et al. Essential role for a long-term depression mechanism in ocular dominance plasticity. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:9860-9865.
2. Dolen G., et al. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013, 501:179-184.
3. Kuzmiski J.B., et al. Metaplasticity of hypothalamic synapses following in vivo challenge. Neuron 2009, 62:839-849.
4. Yin H.H., et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 2009, 12:333-341.
5. Huang C.C., et al. Repeated cocaine administration impairs group II metabotropic glutamate receptor-mediated long-term depression in rat medial prefrontal cortex. J. Neurosci. 2007, 27:2958-2968.
6. Neu A., et al. Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J. Physiol. 2007, 578:233-247.
7. Lodge D., et al. Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors. Neuropharmacology 2013, 74:135-146.
8. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
9. Rodriguez-Moreno A., et al. Presynaptic NMDA receptors and spike timing-dependent depression at cortical synapses. Front. Synaptic Neurosci. 2010, 2:18.
10. Latek D., et al. G protein-coupled receptors - recent advances. Acta Biochim. Pol. 2012, 59:515-529.
11. Betke K.M., et al. GPCR mediated regulation of synaptic transmission. Prog. Neurobiol. 2012, 96:304-321.
12. Oldham W.M., Hamm H.E. Structural basis of function in heterotrimeric G proteins. Q. Rev. Biophys. 2006, 39:117-166.
13. 2+-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J. Neurosci. 1996, 16:1623-1633.
14. 2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar Purkinje cells. J. Neurosci. 2006, 26:86-95.
15. Chen J., et al. Heterosynaptic long-term depression mediated by ATP released from astrocytes. Glia 2013, 61:178-191.
16. Connelly T., et al. Distinct mechanisms contribute to agonist and synaptically induced metabotropic glutamate receptor long-term depression. Eur. J. Pharmacol. 2011, 667:160-168.
17. +-channels in LTD. Eur. J. Neurosci. 2003, 17:1411-1424.
18. Huang C.C., et al. Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J. Physiol. 2001, 532:731-748.
19. Huang Y.C., et al. Mediation of amphetamine-induced long-term depression of synaptic transmission by CB1 cannabinoid receptors in the rat amygdala. J. Neurosci. 2003, 23:10311-10320.
20. 2+ channels in endocannabinoid-mediated long-term depression in the nucleus accumbens. Neuropharmacology 2008, 54:87-94.
21. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J. Neurosci. 2002, 22:4346-4356.
22. 2+-dependent mechanisms involved in presynaptic long-term depression at the hippocampal mossy fibre-CA3 synapse. Eur. J. Neurosci. 1999, 11:1633-1638.
23. 2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. J. Neurophysiol. 1996, 76:2097-2101.
24. Heifets B.D., et al. Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10250-10255.
25. Li S.T., et al. Calcineurin plays different roles in group II metabotropic glutamate receptor- and NMDA receptor-dependent long-term depression. J. Neurosci. 2002, 22:5034-5041.
26. Seino S., Shibasaki T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol. Rev. 2005, 85:1303-1342.
27. Azad S.C., et al. Activation of CB1 specifically located on GABAergic interneurons inhibits LTD in the lateral amygdala. Learn. Mem. 2008, 15:143-152.
28. Chevaleyre V., et al. Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1alpha. Neuron 2007, 54:801-812.
29. Huang C.C., et al. A single in vivo cocaine administration impairs 5-HT(1B) receptor-induced long-term depression in the nucleus accumbens. J. Neurochem. 2013, 125:809-821.
30. Kaeser P.S., Sudhof T.C. RIM function in short- and long-term synaptic plasticity. Biochem. Soc. Trans. 2005, 33:1345-1349.
31. Huang L., et al. Activation of mGluRII induces LTD via activation of protein kinase A and protein kinase C in the dentate gyrus of the hippocampus in vitro. Neuropharmacology 1999, 38:73-83.
32. Kamsler A., et al. Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1618-1623.
33. Pelkey K.A., et al. mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 2005, 46:89-102.
34. Stanton P.K. Transient protein kinase C activation primes long-term depression and suppresses long-term potentiation of synaptic transmission in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1724-1728.
35. Yang J., et al. DGKiota regulates presynaptic release during mGluR-dependent LTD. EMBO J. 2011, 30:165-180.
36. Kahn L., et al. Group 2 metabotropic glutamate receptors induced long term depression in mouse striatal slices. Neurosci. Lett. 2001, 316:178-182.
37. Bender V.A., et al. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci. 2006, 26:4166-4177.
38. Crozier R.A., et al. Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1383-1388.
39. Sjostrom P.J., et al. Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J. Neurophysiol. 2004, 92:3338-3343.
40. Chepkova A.N., et al. Developmental alterations of DHPG-induced long-term depression of corticostriatal synaptic transmission: switch from NMDA receptor-dependent towards CB1 receptor-dependent plasticity. Pflugers Archiv. Eur. J. Physiol. 2009, 459:131-141.
41. Santschi L.A., et al. Activation of receptors negatively coupled to adenylate cyclase is required for induction of long-term synaptic depression at Schaffer collateral-CA1 synapses. J. Neurobiol. 2006, 66:205-219.
42. Upreti C., et al. Role of presynaptic metabotropic glutamate receptors in the induction of long-term synaptic plasticity of vesicular release. Neuropharmacology 2013, 66:31-39.
43. Adermark L., et al. Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur. J. Neurosci. 2009, 29:32-41.
44. Yin H.H., et al. The role of protein synthesis in striatal long-term depression. J. Neurosci. 2006, 26:11811-11820.
45. Zakharenko S.S., et al. Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron 2002, 35:1099-1110.
46. Jung K.M., et al. Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat. Commun. 2012, 3:1080.
47. Tzounopoulos T., et al. A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron 1998, 21:837-845.
48. Johnson K.A., et al. Activation of group II metabotropic glutamate receptors induces long-term depression of excitatory synaptic transmission in the substantia nigra pars reticulata. Neurosci. Lett. 2011, 504:102-106.
49. Kasanetz F., et al. Prefrontal synaptic markers of cocaine addiction-like behavior in rats. Mol. Psychiatry 2013, 18:729-737.
50. Lin H.C., et al. Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J. Neurosci. 2000, 20:9017-9024.
51. 2+ currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 1995, 14:385-397.
52. Zhang X.L., et al. Gbetagamma and the C terminus of SNAP-25 are necessary for long-term depression of transmitter release. PLoS ONE 2011, 6:e20500.
53. Laezza F., et al. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 1999, 285:1411-1414.
54. 2+ channel regulation at divergent mossy-fiber release sites underlies target cell-dependent plasticity. Neuron 2006, 52:497-510.
55. Pelkey K.A., et al. State-dependent cAMP sensitivity of presynaptic function underlies metaplasticity in a hippocampal feedforward inhibitory circuit. Neuron 2008, 60:980-987.
56. Pelkey K.A., McBain C.J. Target-cell-dependent plasticity within the mossy fibre-CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites. J. Physiol. 2008, 586:1495-1502.
57. Kobayashi K., et al. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 1996, 273:648-650.
58. Levenes C., et al. Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J. Physiol. 1998, 510:867-879.
59. Gerdeman G.L., et al. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 2002, 5:446-451.
60. Robbe D., et al. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:8384-8388.
61. Heifets B.D., Castillo P.E. Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol. 2009, 71:283-306.
62. Lovinger D.M., Mathur B.N. Endocannabinoids in striatal plasticity. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S132-S134.
63. Mathur B.N., et al. Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity. Nat. Neurosci. 2013, 16:1275-1283.
64. Younts T.J., Castillo P.E. Endogenous cannabinoid signaling at inhibitory interneurons. Curr. Opin. Neurobiol. 2013, 26C:42-50.
65. Mathur B.N., Lovinger D.M. Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front. Pharmacol. 2012, 3:66.
66. Haj-Dahmane S., Shen R.Y. Regulation of plasticity of glutamate synapses by endocannabinoids and the cyclic-AMP/protein kinase A pathway in midbrain dopamine neurons. J. Physiol. 2010, 588:2589-2604.
67. Kheirbek M.A., et al. Adenylyl cyclase type 5 contributes to corticostriatal plasticity and striatum-dependent learning. J. Neurosci. 2009, 29:12115-12124.
68. 2+ channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol. Pharmacol. 2004, 65:665-674.
69. 2+ channels in cultured rat hippocampal neurons. J. Neurophysiol. 1997, 78:43-50.
70. Robbe D., et al. Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J. Neurosci. 2001, 21:109-116.
71. Yasuda H., et al. Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3106-3111.
72. Azad S.C., et al. Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn. Mem. 2003, 10:116-128.
73. 2+ influx at parallel fibre synapses of the rat cerebellum. J. Physiol. 2004, 557:159-174.
74. Sjostrom P.J., et al. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 2003, 39:641-654.
75. Centonze D., et al. Dopamine, acetylcholine and nitric oxide systems interact to induce corticostriatal synaptic plasticity. Rev. Neurosci. 2003, 14:207-216.
76. Fino E., et al. Asymmetric spike-timing dependent plasticity of striatal nitric oxide-synthase interneurons. Neuroscience 2009, 160:744-754.
77. Wang Y., et al. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 1997, 388:593-598.
78. Grueter B.A., et al. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci. 2010, 13:1519-1525.
79. Tsetsenis T., et al. Rab3B protein is required for long-term depression of hippocampal inhibitory synapses and for normal reversal learning. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14300-14305.
80. Lonart G., et al. Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 2003, 115:49-60.
81. Iremonger K.J., Bains J.S. Retrograde opioid signaling regulates glutamatergic transmission in the hypothalamus. J. Neurosci. 2009, 29:7349-7358.
82. Iremonger K.J., et al. Dual regulation of anterograde and retrograde transmission by endocannabinoids. J. Neurosci. 2011, 31:12011-12020.
83. Wamsteeker Cusulin J.I., et al. Glucocorticoid feedback uncovers retrograde opioid signaling at hypothalamic synapses. Nat. Neurosci. 2013, 16:596-604.
84. Piskorowski R.A., Chevaleyre V. Delta-opioid receptors mediate unique plasticity onto parvalbumin-expressing interneurons in area CA2 of the hippocampus. J. Neurosci. 2013, 33:14567-14578.
85. Atwood B.K., et al. Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum. Nat. Neurosci. 2014, 17:540-548.
86. van den Pol A.N., et al. Neuropeptide Y-mediated long-term depression of excitatory activity in suprachiasmatic nucleus neurons. J. Neurosci. 1996, 16:5883-5895.
87. Mathur B.N., et al. Serotonin induces long-term depression at corticostriatal synapses. J. Neurosci. 2011, 31:7402-7411.
88. Burnstock G., et al. Adenosine and ATP receptors in the brain. Curr. Top. Med. Chem. 2011, 11:973-1011.
89. Dunwiddie T.V., Diao L. Regulation of extracellular adenosine in rat hippocampal slices is temperature dependent: role of adenosine transporters. Neuroscience 2000, 95:81-88.
90. Hosseinmardi N., et al. Theta pulse stimulation: a natural stimulus pattern can trigger long-term depression but fails to reverse long-term potentiation in morphine withdrawn hippocampus area CA1. Brain Res. 2009, 1296:1-14.
91. Sun C.L., et al. Cerebellar long-term depression is deficient in Niemann-Pick type C disease mice. Cerebellum 2011, 10:88-95.
92. Mato S., et al. Presynaptic homeostatic plasticity rescues long-term depression after chronic delta9-tetrahydrocannabinol exposure. J. Neurosci. 2005, 25:11619-11627.
93. Vasquez C., Lewis D.L. The CB1 cannabinoid receptor can sequester G-proteins, making them unavailable to couple to other receptors. J. Neurosci. 1999, 19:9271-9280.
94. Chiu C.Q., et al. Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J. Neurosci. 2010, 30:7236-7248.
95. Pan B., et al. D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J. Neurosci. 2008, 28:14018-14030.
96. Kheder A., Nair K.P. Spasticity: pathophysiology, evaluation and management. Pract. Neurol. 2012, 12:289-298.
97. Munoz A., et al. Combined 5-HT1A and 5-HT1B receptor agonists for the treatment of L-DOPA-induced dyskinesia. Brain 2008, 131:3380-3394.
98. Olive M.F. Metabotropic glutamate receptor ligands as potential therapeutics for addiction. Curr. Drug Abuse Rev. 2009, 2:83-98.
99. Pacher P., Kunos G. Modulating the endocannabinoid system in human health and disease - successes and failures. FEBS J. 2013, 280:1918-1943.
100. Chevaleyre V., et al. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 2006, 29:37-76.
101. Singla S., et al. Mechanisms for synapse specificity during striatal long-term depression. J. Neurosci. 2007, 27:5260-5264.
102. Nahir B., et al. mGluR-mediated and endocannabinoid-dependent long-term depression in the hilar region of the rat dentate gyrus. Neuropharmacology 2010, 58:712-721.
103. Taussig R., et al. Distinct patterns of bidirectional regulation of mammalian adenylyl cyclases. J. Biol. Chem. 1994, 269:6093-6100.
104. 2+ channels by G-protein beta gamma subunits. Nature 1996, 380:258-262.
105. 2+ channels by G-protein beta gamma subunits. Nature 1996, 380:255-258.
106. + channel: expression cloning and molecular properties. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10235-10239.
107. Kretz R., et al. Presynaptic inhibition produced by an identified presynaptic inhibitory neuron. II. Presynaptic conductance changes caused by histamine. J. Neurophysiol. 1986, 55:131-146.
108. + channel in heart. Nature 1987, 325:321-326.
109. Blackmer T., et al. G protein betagamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat. Neurosci. 2005, 8:421-425.
110. 2+ entry. Science 2001, 292:293-297.
111. 2+-dependent binding of synaptotagmin to the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complex. Mol. Pharmacol. 2007, 72:1210-1219.
112. 2+ channels in sensory neurons involves multiple GTP-binding proteins and subunits. Neuron 1995, 14:191-200.
113. Stephens L., et al. A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by G protein beta gamma subunits. Cell 1994, 77:83-93.
114. Pitcher J.A., et al. Role of beta gamma subunits of G proteins in targeting the beta-adrenergic receptor kinase to membrane-bound receptors. Science 1992, 257:1264-1267.
115. Crespo P., et al. Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits. Nature 1994, 369:418-420.
116. Doreulee N., et al. Histamine H(3) receptors depress synaptic transmission in the corticostriatal pathway. Neuropharmacology 2001, 40:106-113.
117. Brown R.E., Haas H.L. On the mechanism of histaminergic inhibition of glutamate release in the rat dentate gyrus. J. Physiol. 1999, 515:777-786.
118. Lin Y., Phillis J.W. Muscarinic agonist oxotremorine-M-induced long-term depression in rat cerebral cortex. Brain Res. Bull. 1991, 27:115-117.
119. Pancani T., et al. M4 mAChR-mediated modulation of glutamatergic transmission at corticostriatal synapses. ACS Chem. Neurosci. 2014, 5:318-324.
120. Ronesi J., et al. Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J. Neurosci. 2004, 24:1673-1679.