Enhanced astroglial Ca2+ signaling increases excitatory synaptic strength in the epileptic brain

GLIA

Volumn 63, Issue 9, 2015, Pages 1507-1521

  Álvarez Ferradas, Carla ^a   Morales, Juan Carlos ^a   Wellmann, Mario ^a   Nualart, Francisco ^b   Roncagliolo, Manuel ^a   Fuenzalida, Marco ^a   Bonansco, Christian ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

Astrocyte; Epilepsy; Gliotransmission; Hippocampus; Kindling; Neurotransmission

Indexed keywords

GLUTAMIC ACID; METABOTROPIC RECEPTOR 5; PURINERGIC P2Y1 RECEPTOR; CALCIUM; DIVALENT CATION; GRM5 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CONTROLLED STUDY; GLUTAMATERGIC SYNAPSE; HIPPOCAMPAL SLICE; MACROGLIA; MALE; NERVE CELL EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE THRESHOLD; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; UPREGULATION; ANIMAL; BRAIN; CHRONIC DISEASE; DISEASE MODEL; DRUG EFFECTS; EPILEPSY, TEMPORAL LOBE; IMMUNOHISTOCHEMISTRY; KINDLING; METABOLISM; PATCH CLAMP TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE; TISSUE CULTURE TECHNIQUE;

ANIMALS; ASTROCYTES; BRAIN; CALCIUM; CATIONS, DIVALENT; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; IMMUNOHISTOCHEMISTRY; KINDLING, NEUROLOGIC; MALE; PATCH-CLAMP TECHNIQUES; RATS, SPRAGUE-DAWLEY; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, PURINERGIC P2Y1; SYNAPSES; SYNAPTIC TRANSMISSION; TISSUE CULTURE TECHNIQUES;

EID: 84949093362     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22817     Document Type: Article

References (60)

1. Angulo MC, Kozlov AS, Charpak S, Audinat E. 2004. Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24:6920-6927.
2. Aronica E, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, Gorter JA. 2000. Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12:2333-2344.
3. Bennett MVL, Garré JM, Orellana JA, Bukauskas FF, Nedergaard M, Giaume C, Sáez JC. 2012. Connexin and pannexin hemichannels in inflammatory responses of glia and neurons. Brain Res 1487:3-15.
4. Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, Van Emde Boas W, Engel J, French J, Glauser TA, Mathern GW, Moshé SL, Nordli D, Plouin P, Scheffer IE. 2010. Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE commission on classification and terminology, 2005-2009. Epilepsia 51:676-685.
5. Bernard C. 2012. Alterations in synaptic function in epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, editors. Jasper's basic mechanisms of the epilepsies, 4th ed. Bethesda, MD: National Center for Biotechnology Information (US). Available at: http://www.ncbi.nlm.nih.gov/books/NBK98161/
6. Boison D, Chen J-F, Fredholm BB. 2010. Adenosine signaling and function in glial cells. Cell Death Differ 17:1071-1082.
7. Bonansco C, Couve A, Perea G, Ferradas CÁ, Roncagliolo M, Fuenzalida M. 2011. Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity. Eur J Neurosci 33:1483-1492.
8. Bonansco C, González de la Vega A, González Alegre P, Borde M, García-Segura LM, Buño W. 2002. Tetanic stimulation of schaffer collaterals induces rhythmic bursts via NMDA receptor activation in rat CA1 pyramidal neurons. Hippocampus 12:434-446.
9. 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 14:1276-1284.
10. Cavus I, Kasoff WS, Cassaday MP, Jacob R, Gueorguieva R, Sherwin RS, Krystal JH, Spencer DD, Abi-Saab WM. 2005. Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann Neurol 57:226-235.
11. Clasadonte J, Haydon PG. 2012. Astrocytes and epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, editors. Jasper's basic mechanisms of the epilepsies, 4th ed. Bethesda, MD: National Center for Biotechnology Information (US). Available at: http://www.ncbi.nlm.nih.gov/books/NBK98159/
12. Cortés-Campos C, Elizondo R, Llanos P, Uranga RM, Nualart F, García MA. 2011. MCT expression and lactate influx/efflux in tanycytes involved in Glia-neuron metabolic interaction. PLoS ONE 6:e16411.
13. Cotrina ML, Lin JH-C, López-García JC, Naus CCG, Nedergaard M. 2000. ATP-mediated glia signaling. J Neurosci 20:2835-2844.
14. Crunelli V, Carmignoto G. 2013. New vistas on astroglia in convulsive and non-convulsive epilepsy highlight novel astrocytic targets for treatment. J Physiol 591:775-785.
15. Cunha RA, Almeida T, Ribeiro JA. 2001. Parallel modification of adenosine extracellular metabolism and modulatory action in the hippocampus of aged rats. J Neurochem 76:372-382.
16. D'Alimonte I, D'Auro M, Citraro R, Biagioni F, Jiang S, Nargi E, Buccella S, Iorio D, Giuliani P, Ballerini P, Caciagli P, Russo FE, Sarro D, Ciccarelli GR. 2009. Altered distribution and function of A2A adenosine receptors in the brain of WAG/rij rats with genetic absence epilepsy, before and after appearance of the disease. Eur J Neurosci 30:1023-1035.
17. Devinsky O, Vezzani A, Najjar S, De Lanerolle NC, Rogawski MA. 2013. Glia and epilepsy: Excitability and inflammation. Trends Neurosci 36:174-184.
18. Dobrunz LE, Stevens CF. 1997. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
19. Domercq M, Brambilla L, Pilati E, Marchaland J, Volterra A, Bezzi P. 2006. P2Y1 Receptor-evoked glutamate exocytosis from astrocytes CONTROL BY TUMOR NECROSIS FACTOR-α and PROSTAGLANDINS. J Biol Chem 281:30684-30696.
20. Fellin T, Gomez-Gonzalo M, Gobbo S, Carmignoto G, Haydon PG. 2006. Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci 26:9312-9322.
21. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G. 2004. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43:729-743.
22. Fields RD, Burnstock G. 2006. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7:423-436.
23. Fonseca CG, Green CR, Nicholson LFB. 2002. Upregulation in astrocytic connexin 43 gap junction levels may exacerbate generalized seizures in mesial temporal lobe epilepsy. Brain Res 929:105-116.
24. Franke H, Verkhratsky A, Burnstock G, Illes P. 2012. Pathophysiology of astroglial purinergic signalling. Purinergic Signal 8:629-657.
25. Fuenzalida M, Aliaga E, Olivares V, Roncagliolo M, Bonansco C. 2009. Developmental increase of asynchronic glutamate release from hippocampal synapses in mutant taiep rat. Synapse 63:502-509.
26. Goddard GV, McIntyre DC, Leech CK. 1969. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol 25:295-330.
27. Gómez-Gonzalo M, Losi G, Chiavegato A, Zonta M, Cammarota M, Brondi M, Vetri F, Uva L, Pozzan T, de Curtis M, Ratto GM, Carmignoto G. 2010. An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol 8:e1000352-
28. Halassa MM, Fellin T, Haydon PG. 2007. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13:54-63.
29. Hsia AY, Malenka RC, Nicoll RA. 1998. Development of excitatory circuitry in the hippocampus. J Neurophysiol 79:2013-2024.
30. Jabs R, Seifert G, Steinhäuser C. 2008. Astrocytic function and its alteration in the epileptic brain. Epilepsia 49:3-12.
31. Jahromi SS, Wentlandt K, Piran S, Carlen PL. 2002. Anticonvulsant actions of gap junctional blockers in an in vitro seizure model. J Neurophysiol 88:1893-1902.
32. 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 10:331-339.
33. Matthias K, Kirchhoff F, Seifert G, Hüttmann K, Matyash M, Kettenmann H, Steinhäuser C. 2003. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23:1750-1758.
34. McNamara JO, Huang YZ, Leonard AS. 2006. Molecular signaling mechanisms underlying epileptogenesis. Sci STKE 2006:re12- Signal Transduct Knowl Environ
35. Morales JC, Álvarez-Ferradas C, Roncagliolo M, Fuenzalida M, Wellmann M, Nualart FJ, Bonansco C. 2014. A new rapid kindling variant for induction of cortical epileptogenesis in freely moving rats. Front Cell Neurosci 8:200.
36. Morimoto K, Fahnestock M, Racine RJ. 2004. Kindling and status epilepticus models of epilepsy: Rewiring the brain. Prog Neurobiol 73:1-60.
37. Nagaraja RY, Becker A, Reymann KG, Balschun D. 2005. Repeated administration of group I mGluR antagonists prevents seizure-induced long-term aberrations in hippocampal synaptic plasticity. Neuropharmacology 49:179-187.
38. Navarrete M, Perea G, Maglio L, Pastor J, Sola RG de, Araque A. 2013. Astrocyte calcium signal and gliotransmission in human brain tissue. Cereb Cortex 23:1240-1246.
39. Notenboom RGE, Hampson DR, Jansen GH, Rijen PC, van Veelen CWM, van Nieuwenhuizen O van, Graan PNEd. 2006. Up-regulation of hippocampal metabotropic glutamate receptor 5 in temporal lobe epilepsy patients. Brain 129:96-107.
40. Orellana JA, von Bernhardi R, Giaume C, Sáez JC. 2012. Glial hemichannels and their involvement in aging and neurodegenerative diseases. Rev Neurosci 23:163-177.
41. Osawa M, Uemura S, Kimura H, Sato M. 2001. Amygdala kindling develops without mossy fiber sprouting and hippocampal neuronal degeneration in rats. Psychiatry Clin Neurosci 55:549-557.
42. Panatier A, Vallée J, Haber M, Murai KK, Lacaille J-C, Robitaille R. 2011. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785-798.
43. Pascual O, Achour SB, Rostaing P, Triller A, Bessis A. 2012. Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci 109:E197-E205.
44. De Paula Cognato G, Bruno AN, Vuaden FC, Sarkis JJF, Bonan CD. 2005. Ontogenetic profile of ectonucleotidase activities from brain synaptosomes of pilocarpine-treated rats. Int J Dev Neurosci 23:703-709.
45. Paxinos G, Watson C. 1998. The rat brain. In: Stereotaxic coordinates, 4th ed. San Diego, CA: Academic Press, Incorporated.
46. Pekny M, Nilsson M. 2005. Astrocyte activation and reactive gliosis. Glia 50:427-434.
47. Perea G, Araque A. 2005. Glial calcium signaling and neuron-glia communication. Cell Calcium 38:375-382.
48. Perea G, Araque A. 2007. Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083-1086.
49. Perea G, Navarrete M, Araque A. 2009. Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci 32:421-431.
50. Perea G, Yang A, Boyden ES, Sur M. 2014. Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat Commun [Internet] 5: Available at: http://www.nature.com/ncomms/2014/140206/ncomms4262/full/ncomms4262.html
51. Racine RJ. 1972. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294.
52. Santiago MF, Veliskova J, Patel NK, Lutz SE, Caille D, Charollais A, Meda P, Scemes E. 2011. Targeting pannexin1 improves seizure outcome. PLoS One 6:e25178.
53. Seifert G, Schilling K, Steinhäuser C. 2006. Astrocyte dysfunction in neurological disorders: A molecular perspective. Nat Rev Neurosci 7:194-206.
54. Shigetomi E, Bowser DN, Sofroniew MV, Khakh BS. 2008. Two forms of astrocyte calcium excitability have distinct effects on NMDA Receptor-mediated slow inward currents in pyramidal neurons. J Neurosci 28:6659-6663.
55. Shi L-H, Luo F, Woodward DJ, McIntyre DC, Chang J-Y. 2007. Temporal sequence of ictal discharges propagation in the corticolimbic basal ganglia system during amygdala kindled seizures in freely moving rats. Epilepsy Res 73:85-97.
56. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
57. Sun W, McConnell E, Pare J-F, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M. 2013. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339:197-200.
58. Tian G-F, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Zielke R, Kang J, Nedergaard M. 2005. An astrocytic basis of epilepsy. Nat Med 11:973-981.
59. Wetherington J, Serrano G, Dingledine R. 2008. Astrocytes in the epileptic brain. Neuron 58:168-178.
60. Zorec R, Araque A, Carmignoto G, Haydon PG, Verkhratsky A, Parpura V. 2012. Astroglial excitability and gliotransmission: An appraisal of Ca2+ as a signalling route. ASN Neuro 4:AN20110061-