Cerebellar ataxia by enhanced Cav2.1 currents is alleviated by Ca2+-dependent K-channel activators in Cacna1aS218l mutant mice

Journal of Neuroscience

Volumn 32, Issue 44, 2012, Pages 15533-15546

  Gao, Zhenyu ^a   Todorov, Boyan ^b   Barrett, Curtis F ^b,d   van Dorp, Stijn ^c   Ferrari, Michel D ^b   van den Maagdenberg, Arn M J M ^b   De Zeeuw, Chris I ^a,c   Hoebeek, Freek E ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d English Editing Solutions   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CACNA1A GENE; CALCIUM CURRENT; CALCIUM TRANSPORT; CEREBELLAR ATAXIA; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; GENE; GENE MUTATION; MALE; MOTOR PERFORMANCE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE CONDUCTANCE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; BENZIMIDAZOLES; CALCIUM; CALCIUM CHANNELS, N-TYPE; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, Q-TYPE; CALCIUM SIGNALING; CEREBELLAR ATAXIA; CHLORZOXAZONE; EXTRACELLULAR SPACE; FEMALE; HOMEOSTASIS; MALE; MICE; MUSCLE RELAXANTS, CENTRAL; MUTATION; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS;

EID: 84868109499     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2454-12.2012     Document Type: Article

References (50)

1. Adams PJ, Rungta RL, Garcia E, van den Maagdenberg AM, MacVicar BA, Snutch TP (2010) Contribution of calcium-dependent facilitation to synaptic plasticity revealed by migraine mutations in the P/Q-type calcium channel. Proc Natl Acad Sci U S A 107:18694-18699.
2. Alviña K, Khodakhah K (2010) KCa channels as therapeutic targets in episodic ataxia type-2. J Neurosci 30:7249-7257.
3. Catterall WA, Dib-Hajj S, Meisler MH, Pietrobon D (2008) Inherited neuronal ion channelopathies: new windows on complex neurological diseases. J Neurosci 28:11768-11777.
4. Cingolani LA, Gymnopoulos M, Boccaccio A, Stocker M, Pedarzani P (2002) Developmental regulation of small-conductance Ca2+-activated K channel expression and function in rat Purkinje neurons. J Neurosci 22: 4456-4467.
5. D'Angelo E, De Filippi G, Rossi P, Taglietti V (1997) Synaptic activation of Ca2+ action potentials in immature rat cerebellar granule cells in situ. J Neurophysiol 78:1631-1642.
6. Davie JT, Clark BA, Häusser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28:7599-7609.
7. 2-dependent K channel. Am J Physiol 271:L775-784.
8. De Zeeuw CI, Hoebeek FE, Bosman LW, Schonewille M, Witter L, Koekkoek SK (2011) Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12:327-344.
9. Edgerton JR, Reinhart PH (2003) Distinct contributions of small and large conductance Ca2+-activated K channels to rat Purkinje neuron function. J Physiol 548:53-69.
10. Eggermont JJ (1990) The correlative brain (Braitenberg, V, ed). New York: Springer.
11. Fletcher CF, Lutz CM, O'Sullivan TN, Shaughnessy JD Jr, Hawkes R, Frankel WN, Copeland NG, Jenkins NA (1996) Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 87:607-617.
12. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
13. Hoebeek FE, Stahl JS, van Alphen AM, Schonewille M, Luo C, Rutteman M, van den Maagdenberg AM, Molenaar PC, Goossens HH, Frens MA, De Zeeuw CI (2005) Increased noise level of purkinje cell activities minimizes impact of their modulation during sensorimotor control. Neuron 45:953-965.
14. Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI (2010) Differential olivocerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A 107:8410-8415.
15. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806-1814.
16. Hounsgaard J, Yamamoto C (1979) Dendritic spikes in Purkinje cells of the guinea pig cerebellum studied in vitro. Exp Brain Res 37:387-398.
17. Jörntell H, Ekerot CF (2006) Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26:11786-11797.
18. 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 calcium channel. Lancet 358:801-807.
19. Kitamura K, Häusser M (2011) Dendritic calcium signaling triggered by spontaneous and sensory-evoked climbing fiber input to cerebellar Purkinje cells in vivo. J Neurosci 31:10847-10858.
20. Kors EE, Terwindt GM, Vermeulen FL, Fitzsimons RB, Jardine PE, Heywood P, Love S, van den Maagdenberg AM, Haan J, Frants RR, Ferrari MD (2001) Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine. Ann Neurol 49:753-760.
21. Kulik A, Nakadate K, Hagiwara A, Fukazawa Y, Luján R, Saito H, Suzuki N, Futatsugi A, Mikoshiba K, Frotscher M, Shigemoto R (2004) Immunocytochemical localization of the alpha 1A subunit of the P/Q-type calcium channel in the rat cerebellum. Eur J Neurosci 19:2169-2178.
22. Llinás R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171-195.
23. Llinás R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197-213.
24. Lonchamp E, Dupont JL, Doussau F, Shin HS, Poulain B, Bossu JL (2009) Deletion of Cav2.1(alpha1(A)) subunit of Ca2+-channels impairs synaptic GABA and glutamate release in the mouse cerebellar cortex in cultured slices. Eur J Neurosci 30:2293-2307.
25. Mark MD, Maejima T, Kuckelsberg D, Yoo JW, Hyde RA, Shah V, Gutierrez D, Moreno RL, Kruse W, Noebels JL, Herlitze S (2011) Delayed postnatal loss of P/Q-type calcium channels recapitulates the absence epilepsy, dyskinesia, and ataxia phenotypes of genomic Cacna1a mutations. J Neurosci 31:4311-4326.
26. McKay BE, Turner RW (2005) Physiological and morphological development of the rat cerebellar Purkinje cell. J Physiol 567:829-850.
27. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, Adams ME (1992) P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 355:827-829.
28. Mittmann W, Häusser M (2007) Linking synaptic plasticity and spike output at excitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27:5559-5570.
29. Mori Y, Wakamori M, Oda S, Fletcher CF, Sekiguchi N, Mori E, Copeland NG, Jenkins NA, Matsushita K, Matsuyama Z, Imoto K (2000) Reduced voltage sensitivity of activation of P/Q-type Ca2+ channels is associated with the ataxic mouse mutation rolling Nagoya (tg(rol)). J Neurosci 20:5654-5662.
30. Ophoff RA, Terwindt GM, Vergouwe MN, van Eijk R, Oefner PJ, Hoffman SM, Lamerdin JE, Mohrenweiser HW, Bulman DE, Ferrari M, Haan J, Lindhout D, van Ommen GJ, Hofker MH, Ferrari MD, Frants RR (1996) Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cell 87:543-552.
31. Pedarzani P, Mosbacher J, Rivard A, Cingolani LA, Oliver D, Stocker M, Adelman JP, Fakler B (2001) Control of electrical activity in central neurons by modulating the gating of small conductance Ca2+-activated K channels. J Biol Chem 276:9762-9769.
32. Pietrobon D (2007) Familial hemiplegic migraine. Neurotherapeutics 4:274-284.
33. Pietrobon D (2010) CaV2.1 channelopathies. Pflugers Arch 460:375-393.
34. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
35. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
36. Rancz EA, Häusser M (2006) Dendritic calcium spikes are tunable triggers of cannabinoid release and short-term synaptic plasticity in cerebellar Purkinje neurons. J Neurosci 26:5428-5437.
37. Schmolesky MT, Weber JT, De Zeeuw CI, Hansel C (2002) The making of a complex spike: ionic composition and plasticity. Ann N Y Acad Sci 978:359-390.
38. Stephens GJ, Morris NP, Fyffe RE, Robertson B (2001) The Cav2.1/alpha1A (P/Q-type) voltage-dependent calcium channel mediates inhibitory neurotransmission onto mouse cerebellar Purkinje cells. Eur J Neurosci 13:1902-1912.
39. Stocker M, Pedarzani P (2000) Differential distribution of three Ca2+-activated K channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci 15:476-493.
40. Stuart G, Häusser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
41. Swensen AM, Bean BP (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23:9650-9663.
42. Szapiro G, Barbour B (2007) Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat Neurosci 10:735-742.
43. Tottene A, Pivotto F, Fellin T, Cesetti T, van den Maagdenberg AM, Pietrobon D (2005) Specific kinetic alterations of human CaV2.1 calcium channels produced by mutation S218L causing familial hemiplegic migraine and delayed cerebral edema and coma after minor head trauma. J Biol Chem 280:17678-17686.
44. van den Maagdenberg AM, Haan J, Terwindt GM, Ferrari MD (2007) Migraine: gene mutations and functional consequences. Curr Opin Neurol 20:299-305.
45. van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, Barrett CF, Gherardini L, van de Ven RC, Todorov B, Broos LA, Tottene A, Gao Z, Fodor M, De Zeeuw CI, Frants RR, Plesnila N, Plomp JJ, Pietrobon D, Ferrari MD (2010) High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann Neurol 67:85-98.
46. Walter JT, Alviña K, Womack MD, Chevez C, Khodakhah K (2006) Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9:389-397.
47. Womack MD, Khodakhah K (2004) Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J Neurosci 24:3511-3521.
48. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoè-Pognetto M, Badura A, Gao Z, Hoebeek FE, van Dorp S, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12:1042-1049.
49. Wylie DR, De Zeeuw CI, Simpson JI (1995) Temporal relations of the complex spike activity of Purkinje cell pairs in the vestibulocerebellum of rabbits. J Neurosci 15:2875-2887.
50. Zhou YD, Turner TJ, Dunlap K (2003) Enhanced G protein-dependent modulation of excitatory synaptic transmission in the cerebellum of the Ca2+ channel-mutant mouse, tottering. J Physiol 547:497-507