Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission

Cerebral Cortex

Volumn 25, Issue 10, 2015, Pages 3699-3712

  Gómez Gonzalo, Marta ^a   Navarrete, Marta ^a,e   Perea, Gertrudis ^a   Covelo, Ana ^b   Martín Fernández, Mario ^b   Shigemoto, Ryuichi ^c   Luján, Rafael ^d   Araque, Alfonso ^a,b  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSITY OF MINNESOTA   (United States)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d Universidad Castilla La Mancha   (Spain)

^e CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Astrocytes; Endocannabinoid signaling; LTP; mGluRs; Nitric oxide

Indexed keywords

ENDOCANNABINOID; GLUTAMIC ACID; METABOTROPIC RECEPTOR; NEUROTRANSMITTER; NITRIC OXIDE; PROTEIN KINASE C; CALCIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ELECTROPHYSIOLOGY; CALCIUM SIGNALING; GLIOTRANSMISSION; HIPPOCAMPAL SLICE; IMMUNOELECTRON MICROSCOPY; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; SYNAPTOSOME; ANIMAL; C57BL MOUSE; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; ASTROCYTES; CALCIUM; ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE, INBRED C57BL; NITRIC OXIDE; PROTEIN KINASE C; PYRAMIDAL CELLS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84947972098     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu231     Document Type: Article

References (71)

1. Agulhon C, Fiacco TA, McCarthy KD. 2010. Hippocampal short-and long-term plasticity are not modulated by astrocyte Ca2+ signaling. Science. 327(5970):1250-1254.
2. Alger BE. 2002. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol. 68 (4):247-286.
3. Anwyl R. 2009. Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology. 56(4):735-740.
4. Araque A, Carmignoto G, Haydon PG. 2001. Dynamic signaling between astrocytes and neurons. Annu Rev Physiol. 63:795-813.
5. Araque A, Martin ED, Perea G, Arellano JI, Buño W. 2002. Synaptically released acetylcholine evokes Ca2+ elevations in astrocytes in hip-pocampal slices. J Neurosci. 22(7):2443-2450.
6. Araque A, Parpura V, Sanzgiri RP, Haydon PG. 1999. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22(5):208-215.
7. Bonansco C, Couve A, Perea G, Ferradas CA, Roncagliolo M, Fuenzalida M. 2011. Glutamate released spontaneously from astro-cytes sets the threshold for synaptic plasticity. Eur J Neurosci. 33 (8):1483-1492.
8. Cachope R, Mackie K, Triller A, O'Brien J, Pereda AE. 2007. Potenti-ation of electrical and chemical synaptic transmission mediated by endocannabinoids. Neuron. 56(6):1034-1047.
9. Carlson G, Wang Y, Alger BE. 2002. Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci. 5(8):723-724.
10. Chevaleyre V, Castillo PE. 2004. Endocannabinoid-mediated metaplas-ticity in the hippocampus. Neuron. 43(6):871-881.
11. Chevaleyre V, Takahashi KA, Castillo PE. 2006. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci. 29:37-76.
12. Crosby KM, Inoue W, Pittman QJ, Bains JS. 2011. Endocannabinoids gate state-dependent plasticity of synaptic inhibition in feeding circuits. Neuron. 71(3):529-541.
13. Daw MI, Chittajallu R, Bortolotto ZA, Dev KK, Duprat F, Henley JM, Collingridge GL, Isaac JT. 2000. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron. 28(3):873-886.
14. Di Castro MA, Chuquet J, Liaudet N, Bhaukaurally K, Santello M, Bouvier D, Tiret P, Volterra A. 2011. Local Ca2+ detection and modulation of synaptic release by astrocytes. Nat Neurosci. 14(10):1276-1284.
15. Dutar P, Nicoll RA. 1988. Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J Neurosci. 8(11):4214-4224.
16. Engisch KL, Wagner JJ, Alger BE. 1996. Whole-cell voltage-clamp investigation of the role of PKC in muscarinic inhibition of IAHP in rat CA1 hippocampal neurons. Hippocampus. 6(2):183-191.
17. Fiacco TA, McCarthy KD. 2004. Intracellular astrocyte calcium waves in situ increase the frequency of spontaneous AMPA receptor currents in CA1 pyramidal neurons. J Neurosci. 24(3):722-732.
18. Fiacco TA, Agulhon C, Taves SR, Petravicz J, Casper KB, Dong X, Chen J, McCarthy KD. 2007. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron. 54(4):611-626.
19. Freund TF, Katona I, Piomelli D. 2003. Role of endogenous cannabi-noids in synaptic signaling. Physiol Rev. 83(3):1017-1066.
20. Han J, Kesner P, Metna-Laurent M, Duan T, Xu L, Georges F, Koehl M, Abrous DN, Mendizabal-Zubiaga J, Grandes P et al. 2012. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell. 148(5):1039-1050.
21. Hardingham N, Dachtler J, Fox K. 2013. The role of nitric oxide in pre-synaptic plasticity and homeostasis. Front Cell Neurosci. 7:190.
22. Hawkins RD, Son H, Arancio O. 1998. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res. 118:155-172.
23. Haydon PG, Carmignoto G. 2006. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev. 86(3):1009-1031.
24. Heifets BD, Castillo PE. 2009. Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol. 71:283-306.
25. Henneberger C, Papouin T, Oliet SH, Rusakov DA. 2010. Long-term potentiation depends on release of D-serine from astrocytes. Nature. 463(7278):232-236.
26. Isaac JT, Hjelmstad GO, Nicoll RA, Malenka RC. 1996. Long-term potentiation at single fiber inputs to hippocampal CA1 pyramidal cells. Proc Natl Acad Sci USA. 93(16):8710-8715.
27. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, Domercq M, Matute C, Tonello F, Gundersen V, Volterra A. 2007. Glutamate exocytosis from astrocytes controls synaptic strength. Nat Neurosci. 10(3):331-339.
28. Kang J, Jiang L, Goldman SA, Nedergaard M. 1998. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci. 1 (8):683-692.
29. Kishimoto Y, Fujimichi R, Araishi K, Kawahara S, Kano M, Aiba A, Kirino Y. 2002. mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur J Neurosci. 16(12):2416-2424.
30. Kreitzer AC, Regehr WG. 2001b. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabi-noids. J Neurosci. 21(20):RC174.
31. Kreitzer AC, Regehr WG. 2001a. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 29(3):717-727.
32. Kwon HB, Castillo PE. 2008. Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron. 57(1):108-120.
33. Li X, Zima AV, Sheikh F, Blatter LA, Chen J. 2005. Endothelin-1-induced arrhythmogenic Ca2+ signaling is abolished in atrial myocytes of inositol-1, 4, 5-trisphosphate(IP3)-receptor type 2-deficient mice. Circ Res. 96(12):1274-1281.
34. Ling DS, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, Sacktor TC. 2002. Protein kinase Mzeta is necessary and sufficient for LTP maintenance. Nat Neurosci. 5(4):295-296.
35. Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P. 1996. Perisy-naptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci. 8(7):1488-1500.
36. Maldonado R, Valverde O, Berrendero F. 2006. Involvement of the en-docannabinoid system in drug addiction. Trends Neurosci. 29 (4):225-232.
37. Martin ED, Araque A, Buno W. 2001. Synaptic regulation of the slow Ca2+-activated K+ current in hippocampal CA1 pyramidal neurons: implication in epileptogenesis. J Neurophysiol. 86(6):2878-2886.
38. Martineau M, Baux G, Mothet JP. 2006. D-serine signalling in the brain: friend and foe. Trends Neurosci. 29(8):481-491.
39. Min R, Nevian T. 2012. Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci. 15 (5):746-753.
40. Navarrete M, Araque A. 2008. Endocannabinoids mediate neuron-astrocyte communication. Neuron. 57(6):883-893.
41. Navarrete M, Araque A. 2010. Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron. 68(1):113-126.
42. Navarrete M, Perea G, Fernandez de Sevilla D, Gómez-Gonzalo M, Núñez A, Martín ED, Araque A. 2012. Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol. 10(2):e1001259.
43. Nedergaard M, Ransom B, Goldman SA. 2003. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26(10):523-530.
44. Nett WJ, Oloff SH, McCarthy KD. 2002. Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol. 87(1):528-537.
45. Ohno-Shosaku T, Maejima T, Kano M. 2001. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron. 29(3):729-738.
46. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M. 2002. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippo-campal synapses. J Neurosci. 22(10):3864-3872.
47. Panatier A, Vallée J, Haber M, Murai KK, Lacaille JC, Robitaille R. 2011. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell. 146(5):785-798.
48. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH. 2006. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell. 125(4):775-784.
49. Parpura V, Zorec R. 2010. Gliotransmission: exocytotic release from as-trocytes. Brain Res Rev. 63(1-2):83-92.
50. Parri HR, Gould TM, Crunelli V. 2001. Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci. 4(8):803-812.
51. Perea G, Araque A. 2007. Astrocytes potentiate transmitter release at single hippocampal synapses. Science. 317(5841):1083-1086.
52. Perea G, Araque A. 2005. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci. 25(9):2192-2203.
53. Perea G, Navarrete M, Araque A. 2009. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32 (8):421-431.
54. Petravicz J, Fiacco TA, McCarthy KD. 2008. Loss of IP3 receptor-dependent Ca2+ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J Neurosci. 28(19):4967-4973.
55. Piomelli D. 2003. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci. 4(11):873-884.
56. Raastad M. 1995. Extracellular activation of unitary excitatory synapses between hippocampal CA3 and CA1 pyramidal cells. Eur J Neuros-ci. 7(9):1882-1888.
57. Rodriguez-Moreno A, Sistiaga A, Lerma J, Sánchez-Prieto J. 1998. Switch from facilitation to inhibition of excitatory synaptic transmission by group I mGluR desensitization. Neuron. 21(6):1477-1486.
58. Sanchez-Prieto J, Paternain AV, Lerma J. 2004. Dual signaling by mGluR5a results in bi-directional modulation of N-type Ca2+ channels. FEBS Lett. 576(3):428-432.
59. Schuman EM, Madison DV. 1994. Nitric oxide and synaptic function. Annu Rev Neurosci. 17:153-183.
60. Schuman EM, Madison DV. 1991. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science. 254 (5037):1503-1506.
61. Seroussi Y, Brosh I, Barkai E. 2002. Learning-induced reduction in post-burst after-hyperpolarization (AHP) is mediated by activation of PKC. Eur J Neurosci. 16(5):965-969.
62. Singh P, Jorgacevski J, Kreft M, Grubišić V, Stout RF Jr, Potokar M, Parpura V, Zorec R. 2014. Single-vesicle architecture of synaptobre-vin2 in astrocytes. Nat Commun. 5:3780.
63. Song J, Kyriakatos A, El Manira A. 2012. Gating the polarity of endocannabinoid-mediated synaptic plasticity by nitric oxide in the spinal locomotor network. J Neurosci. 32(15):5097-5105.
64. Takata N, Mishima T, Hisatsune C, Nagai T, Ebisui E, Mikoshiba K, Hirase H. 2011. Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J Neurosci. 31(49):18155-18165.
65. Tamagnini F, Barker G, Warburton EC, Burattini C, Aicardi G, Bashir ZI. 2013. Nitric oxide-dependent long-term depression but not endocannabinoid-mediated long-term potentiation is crucial for visual recognition memory. J Physiol. 591(Pt 16):3963-3979.
66. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F et al. 1991. The bisin-dolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem. 266(24):15771-15781.
67. Volterra A, Meldolesi J. 2005. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci. 6 (8):626-640.
68. Wilson RI, Nicoll RA. 2002. Endocannabinoid signaling in the brain. Science. 296(5568):678-682.
69. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 410(6828):588-592.
70. Xu JY, Zhang J, Chen C. 2012. Long-lasting potentiation of hippocam-pal synaptic transmission by direct cortical input is mediated via en-docannabinoids. J Physiol. 590(Pt 10):2305-2315.
71. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI. 1999. Increased mortality, hypoactivity, and hypoalgesia in canna-binoid CB1 receptor knockout mice. Proc Natl Acad Sci USA. 96 (10):5780-5785.