Calcium signaling and epilepsy

Cell and Tissue Research

Volumn 357, Issue 2, 2014, Pages 385-393

  Steinlein, Ortrud K ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Calcium signaling; Epilepsy; Gliotransmission; Hyperexcitability; Seizures

Indexed keywords

CALCIUM;

ANIMAL; CALCIUM SIGNALING; EPILEPSY; GENETICS; HUMAN; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CALCIUM; CALCIUM SIGNALING; EPILEPSY; HUMANS; MUTATION; NEURONS;

EID: 84905918844     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1849-1     Document Type: Review

References (91)

1. Abel T, Nguyen PV, Barad M, Deuel TAS, Kandel ER (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626 (Pubitemid 27152404)
2. Achyuthan KE, Greenberg CS (1987) Identification of a guanosine triphosphate-binding site on Guinea-pig liver transglutaminase - role of Gtp and calcium-ions in modulating activity. J Biol Chem 262:1901-1906
3. Aronica E, Zurolo E, Iyer A, de Groot M, Anink J, Carbonell C, van Vliet EA, Baayen JC, Boison D, Gorter JA (2011) Upregulation of adenosine kinase in astrocytes in experimental and human temporal lobe epilepsy. Epilepsia 52:1645-1655
4. Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325-337 (Pubitemid 37021228)
5. Arundine M, Aarts M, Lau A, Tymianski M (2004) Vulnerability of central neurons to secondary insults after in vitro mechanical stretch. J Neurosci 24:8106-8123 (Pubitemid 39280831)
6. Bading H (2013) Nuclear calcium signalling in the regulation of brain function. Nat Rev Neurosci 14:593-608
7. Berkefeld H, Sailer CA, Bildl W, Rohde V, Thumfart JO, Eble S, Klugbauer N, Reisinger E, Bischofberger J, Oliver D et al (2006) BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science 314:615-620 (Pubitemid 44646378)
8. Blackburn D, Sargsyan S, Monk PN, Shaw PJ (2009) Astrocyte function and role in motor neuron disease: a future therapeutic target? Glia 57:1251-1264
9. Brookes PS, Yoon YS, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 287:C817-C833 (Pubitemid 39238305)
10. Carmignoto G, Haydon PG (2012) Astrocyte calcium signaling and epilepsy. Glia 60:1227-1233
11. Chan YC, Burgunder JM, Wilder-Smith E, Chew SE, Lam-Mok-Sing KM, Sharma V, Ong BK (2008) Electroencephalographic changes and seizures in familial hemiplegic migraine patients with the CACNA1A gene S218L mutation. J Clin Neurosci 15:891-894
12. Chen Y, Lu J, Pan H, Zhang Y, Wu H, Xu K, Liu X, Jiang Y, Bao X, Yao Z et al (2003) Association between genetic variation of CACNA1H and childhood absence epilepsy. Ann Neurol 54:239-243 (Pubitemid 36909623)
13. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N (2009) Translational control of long-lasting synaptic plasticity and memory. Neuron 61:10-26
14. Curtain RP, Smith RL, Ovcaric M, Griffiths LR (2006) Minor head trauma-induced sporadic hemiplegic migraine coma. Pediatr Neurol 34:329-332
15. Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10:456-465 (Pubitemid 37499775)
16. David Y, Cacheaux LP, Ivens S, Lapilover E, Heinemann U, Kaufer D, Friedman A (2009) Astrocytic dysfunction in epileptogenesis: consequence of altered potassium and glutamate homeostasis? J Neurosci 29:10588-10599
17. Debiais S, Hommet C, Bonnaud I, Barthez MA, Rimbaux S, Riant F, Autret A (2009) The FHM1 mutation S218L: a severe clinical phenotype? A case report and review of the literature. Cephalalgia 29:1337-1339
18. DeLorenzo RJ, Sun DA, Deshpande LS (2005) Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintainance of epilepsy. Pharmacol Ther 105:229-266 (Pubitemid 40297893)
19. Dietzel I, Heinemann U, Lux HD (1989) Relations between slow extracellular potential changes, glial potassium buffering, and electrolyte and cellular-volume changes during neuronal hyperactivity in cat brain. Glia 2:25-44
20. Ernst WL, Zhang Y, Yoo JW, Ernst SJ, Noebels JL (2009) Genetic enhancement of thalamocortical network activity by elevating alpha 1g-mediated low-voltage-activated calcium current induces pure absence epilepsy. J Neurosci 29:1615-1625
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 (Pubitemid 39179731)
22. 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 (Pubitemid 44359857)
23. Gao Z, Todorov B, Barrett CF, van Dorp S, Ferrari MD, van den Maagdenberg AM, De Zeeuw CI, Hoebeek FE (2012) Cerebellar ataxia by enhanced Ca(V)2.1 currents is alleviated by Ca2+-dependent K+-channel activators in Cacna1a(S218L) mutant mice. J Neurosci 32:15533-15546
24. Gomez-Gonzalo M, Losi G, Chiavegato A, Zonta M, Cammarota M, Brondi M, Vetri F, Uva L, Pozzan T, de Curtis M et al (2010) An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol 8:e1000352
25. Greer PL, Greenberg ME (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59:846-860
26. Guemez-Gamboa A, Estrada-Sanchez AM, Montiel T, Paramo B, Massieu L, Moran J (2011) Activation of NOX2 by the stimulation of ionotropic and metabotropic glutamate receptors contributes to glutamate neurotoxicity in vivo through the production of reactive oxygen species and calpain activation. J Neuropathol Exp Neurol 70:1020-1035
27. Gurkoff GG, Shahlaie K, Lyeth BG (2012) In vitro mechanical strain trauma alters neuronal calcium responses: implications for posttraumatic epilepsy. Epilepsia 53:53-60
28. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, Jin H, Wang X, Rosenberg GA, Lo EH, Moskowitz MA (2004) Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 113:1447-1455 (Pubitemid 39071700)
29. Hartmann J, Konnerth A (2005) Determinants of postsynaptic Ca2+ signaling in Purkinje neurons. Cell Calcium 37:459-466 (Pubitemid 40458443)
30. Hawk JD, Abel T (2011) The role of NR4A transcription factors in memory formation. Brain Res Bull 85:21-29
31. Heinemann U, Gabriel S, Schuchmann S, Eder C (1999) Contribution of astrocytes to seizure activity. Adv Neurol 79:583-590
32. Heron SE, Phillips HA, Mulley JC, Mazarib A, Neufeld MY, Berkovic SF, Scheffer IE (2004) Genetic variation of CACNA1H in idiopathic generalized epilepsy. Ann Neurol 55:595-596 (Pubitemid 38391980)
33. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y (2001) An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281:C922-C931
34. Hirschberg B, Maylie J, Adelman JP, Marrion NV (1999) Gating properties of single SK channels in hippocampal CA1 pyramidal neurons. Biophys J 77:1905-1913 (Pubitemid 29463152)
35. Hulme JT, Lin TWC, Westenbroek RE, Scheuer T, Catterall WA (2003) beta-adrenergic regulation requires direct anchoring of PKA to cardiac Ca(V)1.2 channels via a leucine zipper interaction with A kinase-anchoring protein 15. Proc Natl Acad Sci USA 100:13093-13098 (Pubitemid 37340031)
36. Imbrici P, Jaffe SL, Eunson LH, Davies NP, Herd C, Robertson R, Kullmann DM, Hanna MG(2004) Dysfunction of the brain calcium channel CaV2.1 in absence epilepsy and episodic ataxia. Brain 127:2682-2692 (Pubitemid 39627377)
37. Jodice C, Mantuano E, Veneziano L, Trettel F, Sabbadini G, Calandriello L, Francia A, Spadaro M, Pierelli F, Salvi F et al (1997) Episodic ataxia type 2 (EA2) and spinocerebellar ataxia type 6 (SCA6) due to CAG repeat expansion in the CACNA1A gene on chromosome 19p. Hum Mol Genet 6:1973-1978 (Pubitemid 27460375)
38. Jouvenceau A, Eunson LH, Spauschus A, Ramesh V, Zuberi SM, Kullmann DM, Hanna MG (2001) Human epilepsy associated with dysfunction of the brain P/Q-type calciumchannel. Lancet 358:801-807 (Pubitemid 32868732)
39. Jun K, Piedras-Renteria ES, Smith SM, Wheeler DB, Lee SB, Lee TG, Chin H, Adams ME, Scheller RH, Tsien RW et al (1999) Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci USA 96:15245-15250 (Pubitemid 30019797)
40. Khosravani H, Zamponi GW(2006) Voltage-gated calcium channels and idiopathic generalized epilepsies. Physiol Rev 86:941-966 (Pubitemid 44033386)
41. Kors EE, Terwindt GM, Vermeulen FL, Fitzsimons RB, Jardine PE, Heywood P, Love S, van den Maagdenberg AM, Haan J, Frants RR et al (2001) Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationshipwith familial hemiplegicmigraine. Ann Neurol 49:753-760 (Pubitemid 32530242)
42. Kovacs R, Szilagyi N, Barabas P, Heinemann U, Kardos J (2000) Low-[Mg2+]-induced Ca2+ fluctuations in organotypic hippocampal slice cultures. Neuroreport 11:2107-2111 (Pubitemid 30485544)
43. Kovacs R, Schuchmann S, Gabriel S, Kann O, Kardos J, Heinemann U (2002) Free radical-mediated cell damage after experimental status epilepticus in hippocampal slice cultures. J Neurophysiol 88:2909-2918 (Pubitemid 35448678)
44. Kunz WS, Goussakov IV, Beck H, Elger CE (1999) Altered mitochondrial oxidative phosphorylation in hippocampal slices of kainate-treated rats. Brain Res 826:236-242 (Pubitemid 29222938)
45. Lee CJ, Mannaioni G, Yuan H, Woo DH, Gingrich MB, Traynelis SF (2007) Astrocytic control of synaptic NMDA receptors. J Physiol 581:1057-1081 (Pubitemid 46887980)
46. Li L, Head V, Timpe LC (2001) Identification of an inward rectifier potassium channel gene expressed in mouse cortical astrocytes. Glia 33:57-71 (Pubitemid 32102817)
47. Liang J, Zhang Y, Wang J, Pan H, Wu H, Xu K, Liu X, Jiang Y, Shen Y, Wu X (2006) New variants in the CACNA1H gene identified in childhood absence epilepsy. Neurosci Lett 406:27-32 (Pubitemid 44403895)
48. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190 (Pubitemid 135706588)
49. Lorenzon NM, Lutz CM, Frankel WN, Beam KG (1998) Altered calcium channel currents in Purkinje cells of the neurological mutant mouse leaner. J Neurosci 18:4482-4489 (Pubitemid 28280159)
50. Losi G, Cammarota M, Chiavegato A, Gomez-Gonzalo M, Carmignoto G (2010) A new experimental model of focal seizures in the entorhinal cortex. Epilepsia 51:1493-1502
51. Maragakis NJ, Rothstein JD (2006) Mechanisms of disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2:679-689 (Pubitemid 44782682)
52. Miki T, Zwingman TA, Wakamori M, Lutz CM, Cook SA, Hosford DA, Herrup K, Fletcher CF, Mori Y, Frankel WN et al (2008) Two novel alleles of tottering with distinct Ca(v)2.1 calcium channel neuropathologies. Neuroscience 155:31-44
53. Morris TA, Jafari N, Rice AC, Vasconcelos O, DeLorenzo RJ (1999) Persistent increased DNA-binding and expression of serum response factor occur with epilepsy-associated long-term plasticity changes. J Neurosci 19:8234-8243 (Pubitemid 30226742)
54. Nakamura K, Kodera H, Akita T, Shiina M, Kato M, Hoshino H, Terashima H, Osaka H, Nakamura S, Tohyama J et al (2013) De Novo mutations in GNAO1, encoding a Galphao subunit of heterotrimeric G proteins, cause epileptic encephalopathy. Am J Hum Genet 93:496-505
55. Newman EA (1993) Inward-rectifying potassium channels in retinal glial (Muller) cells. J Neurosci 13:3333-3345
56. Niespodziany I, Klitgaard H, Margineanu DG (2001) Levetiracetam inhibits the high-voltage-activated Ca2+ current in pyramidal neurones of rat hippocampal slices. Neurosci Lett 306:5-8 (Pubitemid 32524284)
57. Noebels JL (1986) Mutational analysis of inherited epilepsies. Adv Neurol 44:97-113
58. Noebels JL (2012) The voltage-gated calcium channel and absence epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV (eds) Jasper's Basic Mechanisms of the Epilepsies, 4th edn. Oxford University Press, New York, pp 702-713
59. Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Oefner PJ, Hoffman SM, Lamerdin JE, Mohrenweiser HW, Bulman DE, Ferrari M et al (1996) Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 87:543-552 (Pubitemid 26374327)
60. Ozcan M, Ayar A (2012) Modulation of action potential and calcium signaling by levetiracetam in rat sensory neurons. J Recept Signal Transduct Res 32:156-162
61. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369:744-747 (Pubitemid 24225363)
62. Patel M (2004) Mitochondrial dysfunction and oxidative stress: cause and consequence of epileptic seizures. Free Radical Biol Med 37:1951-1962
63. Pedley TA, Fisher RS, Futamachi KJ, Prince DA (1976) Regulation of extracellular potassium concentration in epileptogenesis. Fed Proc 35:1254-1259
64. Perez-Campo R, Lopez-Torres M, Cadenas S, Rojas C, Barja G (1998) The rate of free radical production as a determinant of the rate of aging: evidence from the comparative approach. J Comp Physiol B 168:149-158 (Pubitemid 28202995)
65. Pitkanen A, Lukasiuk K (2009) Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav 14:16-25
66. Poopalasundaram S, Knott C, Shamotienko OG, Foran PG, Dolly JO, Ghiani CA, Gallo V, Wilkin GP (2000) Glial heterogeneity in expression of the inwardly rectifying K(+) channel, Kir4.1, in adult rat CNS. Glia 30:362-372 (Pubitemid 30334337)
67. Ransom CB, Sontheimer H (1995) Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol 73:333-346
68. Reato D, Cammarota M, Parra LC, Carmignoto G (2012) Computational model of neuron-astrocyte interactions during focal seizure generation. Front Comput Neurosci 6:81
69. Seifert G, Huttmann K, Binder DK, Hartmann C, Wyczynski A, Neusch C, Steinhauser C (2009) Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 29:7474-7488
70. Shahlaie K, Lyeth BG, Gurkoff GG, Muizelaar JP, Berman RF (2010) Neuroprotective effects of selective N-type VGCC blockade on stretch-injury-induced calcium dynamics in cortical neurons. J Neurotrauma 27:175-187
71. Shalin SC, Hernandez CM, Dougherty MK, Morrison DK, Sweatt JD (2006) Kinase suppressor of Ras1 compartmentalizes hippocampal signal transduction and subserves synaptic plasticity and memory formation. Neuron 50:765-779 (Pubitemid 43775734)
72. 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
73. Singh B, Monteil A, Bidaud I, Sugimoto Y, Suzuki T, Hamano S, Oguni H, Osawa M, Alonso ME, Delgado-Escueta AV et al (2007) Mutational analysis of CACNA1G in idiopathic generalized epilepsy. Mutation in brief #962. Online. Hum Mutat 28:524-525
74. Smethurst PA, Griffin M (1996) Measurement of tissue transglutaminase activity in a permeabilized cell system: its regulation by Ca2+ and nucleotides. Biochem J 313:803-808
75. Su H, Sochivko D, Becker A, Chen J, Jiang YW, Yaari Y, Beck H (2002) Upregulation of a T-type Ca2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J Neurosci 22:3645-3655 (Pubitemid 37465769)
76. Takahashi E, Niimi K, Itakura C (2010) Levetiracetam-mediated emotional behavior in heterozygous rolling Nagoya Ca(V)2.1 channel mutant mice. Pharmacol Biochem Behav 96:294-300
77. Tanaka K (2001) Alteration of second messengers during acute cerebral ischemia - adenylate cyclase, cyclic AMP-dependent protein kinase, and cyclic AMP response element binding protein. Prog Neurobiol 65:173-207
78. Thomas E, Grisar T (2000) Increased synchrony with increase of a low-threshold calcium conductance in a model thalamic network: a phase-shift mechanism. Neural Comput 12:1553-1571
79. Tian GF, Azmi H, Takano T, Xu Q, Peng W, Lin J, Oberheim N, Lou N, Wang X, Zielke HR et al (2005) An astrocytic basis of epilepsy. Nat Med 11:973-981 (Pubitemid 41294443)
80. Torres A, Wang F, Xu Q, Fujita T, Dobrowolski R, Willecke K, Takano T, Nedergaard M (2012) Extracellular Ca(2)(+) acts as a mediator of communication from neurons to glia. Sci Signal 5:ra8
81. Tostevin F, ten Wolde PR, Howard M (2007) Fundamental limits to position determination by concentration gradients. Plos Comput Biol 3:763-771 (Pubitemid 46683458)
82. Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D (2002) Familial hemiplegic migraine mutations increase Ca(2+) influx through single human CaV2.1 channels and decrease maximal CaV2.1 current density in neurons. Proc Natl Acad Sci USA 99:13284-13289
83. Tucholski J, Roth KA, Johnson GVW (2006) Tissue transglutaminase overexpression in the brain potentiates calcium-induced hippocampal damage. J Neurochem 97:582-594
84. Ulas J, Satou T, Ivins KJ, Kesslak JP, Cotman CW, Balazs R (2000) Expression of metabotropic glutamate receptor 5 is increased in astrocytes after kainate-induced epileptic seizures. Glia 30:352-361 (Pubitemid 30334336)
85. Vitko I, Bidaud I, Arias JM, Mezghrani A, Lory P, Perez-Reyes E (2007) The I-II loop controls plasma membrane expression and gating of Ca(v)3.2 T-type Ca2+ channels: a paradigm for childhood absence epilepsy mutations. J Neurosci 27:322-330 (Pubitemid 46106006)
86. Vizi ES, Kisfali M, Lorincz T (2013) Role of nonsynaptic GluN2B-containing NMDA receptors in excitotoxicity: evidence that fluoxetine selectively inhibits these receptors and may have neuroprotective effects. Brain Res Bull 93:32-38
87. Waldbaum S, Patel M (2010) Mitochondrial dysfunction and oxidative stress: a contributing link to acquired epilepsy? J Bioenerg Biomembr 42:449-455
88. Wallraff A, Kohling R, Heinemann U, Theis M, Willecke K, Steinhauser C (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26:5438-5447 (Pubitemid 44318396)
89. Weber JT, Rzigalinski BA, Willoughby KA, Moore SF, Ellis EF (1999) Alterations in calcium-mediated signal transduction after traumatic injury of cortical neurons. Cell Calcium 26:289-299 (Pubitemid 30037830)
90. Xie G, Clapcote SJ, Nieman BJ, Tallerico T, Huang Y, Vukobradovic I, Cordes SP, Osborne LR, Rossant J, Sled JG et al (2007) Forward genetic screen of mouse reveals dominant missense mutation in the P/Q-type voltage-dependent calcium channel, CACNA1A. Genes Brain Behav 6:717-727 (Pubitemid 350043943)
91. Zwingman TA, Neumann PE, Noebels JL, Herrup K (2001) Rocker is a new variant of the voltage-dependent calcium channel gene Cacna1a. J Neurosci 21:1169-1178 (Pubitemid 32128762)