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Di Guilmi, M.N.; Wang, T.; Inchauspe, C.G.; Forsythe, I.D.; Ferrari, M.D.; Van Der Maagdenberg, A.M.J.M.; Borst, J.G.G.; Uchitel, O.D. "Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i" (2014) Journal of Neuroscience. 34(21):7047-7058
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Abstract:

Specific missense mutations in the CACNA1A gene, which encodes a subunit of voltage-gated CaV2.1 channels, are associated with familial hemiplegic migraine type 1 (FHM1), a rare monogenic subtype of common migraine with aura. We used transgenic knock-in (KI) mice harboring the human pathogenic FHM1 mutation S218L to study presynaptic Ca 2 currents, EPSCs, and in vivo activity at the calyx of Held synapse. Whole-cell patch-clamp recordings of presynaptic terminals from S218L KI mice showed a strong shift of the calcium current I-V curve to more negative potentials, leading to an increase in basal [Ca 2]i, increased levels of spontaneous transmitter release, faster recovery from synaptic depression, and enhanced synaptic strength despite smaller action-potential-elicited Ca 2 currents. The gain-of-function of transmitter release of the S218L mutant was reproduced in vivo, including evidence for an increased release probability, demonstrating its relevance for glutamatergic transmission. This synaptic phenotype may explain the misbalance between excitation and inhibition in neuronal circuits resulting in a persistent hyperexcitability state and other migraine-relevant mechanisms such as an increased susceptibility to cortical spreading depression. © 2014 the authors.

Registro:

Documento: Artículo
Título:Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i
Autor:Di Guilmi, M.N.; Wang, T.; Inchauspe, C.G.; Forsythe, I.D.; Ferrari, M.D.; Van Der Maagdenberg, A.M.J.M.; Borst, J.G.G.; Uchitel, O.D.
Filiación:Institute of Physiology, Molecular Biology and Neuroscience (IFIBYNE, UBA-CONICET), Department of Physiology, Molecular, and Cell Biology, University of Buenos Aires, Buenos Aires C1428EHA, Argentina
Department of Neuroscience, Erasmus MC, University Medical Center, Rotterdam NL-3000 CA, Netherlands
Neurotoxicity at the Synaptic Interface, Medical Research Council Toxicology Unit, University of Leicester, Leicester LE1 9HN, United Kingdom
Department of Neurology, Leiden University Medical Center, Leiden 2300 RC, Netherlands
Department of Human Genetics, Leiden University Medical Center, Leiden 2300 RC, Netherlands
Palabras clave:Calyx of Held; FHM-1; In vivo; P/Q calcium channels; Synaptic transmission; unclassified drug; voltage gated calcium channel; voltage gated calcium channel 2.1; action potential; adult; animal experiment; animal model; animal tissue; article; auditory stimulation; calcium current; calyx of held; controlled study; electrophysiology; excitatory postsynaptic potential; familial hemiplegic migraine; gain of function mutation; mouse; neurotransmitter release; nonhuman; presynaptic membrane; priority journal; synapse; synaptic transmission; whole cell patch clamp; calyx of Held; FHM-1; in vivo; P/Q calcium channels; synaptic transmission; Agatoxins; Animals; Brain Stem; Calcium; Calcium Channels, N-Type; Disease Models, Animal; Humans; Mice; Mice, Inbred C57BL; Mice, Transgenic; Migraine with Aura; Mutation; Neurotoxins; Sodium Channel Blockers; Synapses; Tetrodotoxin; Time Factors
Año:2014
Volumen:34
Número:21
Página de inicio:7047
Página de fin:7058
DOI: http://dx.doi.org/10.1523/JNEUROSCI.2526-13.2014
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.
ISSN:02706474
CODEN:JNRSD
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02706474_v34_n21_p7047_DiGuilmi

Referencias:

  • Adams, P.J., Rungta, R.L., Garcia, E., van den Maagdenberg, A.M., Macvicar, B.A., Snutch, T.P., Contribution of calcium-dependent facilitation to synaptic plasticity revealed by migraine mutations in the P/Q-type calcium channel (2010) Proc Natl Acad Sci U S A, 107, pp. 18694-18699. , CrossRef Medline
  • Awatramani, G.B., Price, G.D., Trussell, L.O., Modulation of transmitter release by presynaptic resting potential and background calcium levels (2005) Neuron, 48, pp. 109-121. , CrossRef Medline
  • Bacaj, T., Wu, D., Yang, X., Morishita, W., Zhou, P., Xu, W., Malenka, R.C., Sudhof, T.C., Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release (2013) Neuron, 80, pp. 947-959. , CrossRef Medline
  • Borst, J.G.G., Sakmann, B., Facilitation of presynaptic calcium currents in the rat brainstem (1998) J Physiol, 513, pp. 149-155. , CrossRef Medline
  • Borst, J.G.G., Helmchen, F., Sakmann, B., Pre-and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat (1995) J Physiol, 489, pp. 825-840. , Medline
  • Bouhours, B., Trigo, F.F., Marty, A., Somatic depolarization enhances GABA release in cerebellar interneurons via a calcium/protein kinase Cpathway (2011) J Neurosci, 31, pp. 5804-5815. , CrossRef Medline
  • Catterall, W.A., Dib-Hajj, S., Meisler, M.H., Pietrobon, D., Inherited neuronal ion channelopathies: New windows on complex neurological diseases (2008) J Neurosci, 28, pp. 11768-11777. , CrossRef Medline
  • Chan, Y.C., Burgunder, J.M., Wilder-Smith, E., Chew, S.E., Lam-Mok-Sing, K.M., Sharma, V., Ong, B.K., Electroencephalographic changes and seizures in familial hemiplegic migraine patients with the CACNA1A gene S218L mutation (2008) J Clin Neurosci, 15, pp. 891-894. , CrossRef Medline
  • Chu, Y., Fioravante, D., Thanawala, M., Leitges, M., Regehr, W.G., Calcium-dependent isoforms of protein kinase C mediate glycineinduced synaptic enhancement at the calyx of Held (2012) J Neurosci, 32, pp. 13796-13804. , CrossRef Medline
  • Crins, T.T., Rusu, S.I., Rodríguez-Contreras, A., Borst, J.G.G., Developmental changes in short-term plasticity at the rat calyx of Held synapse (2011) J Neurosci, 31, pp. 11706-11717. , CrossRef Medline
  • Cuttle, M.F., Tsujimoto, T., Forsythe, I.D., Takahashi, T., Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem (1998) J Physiol, 512, pp. 723-729. , CrossRef Medline
  • de Vries, B., Frants, R.R., Ferrari, M.D., van den Maagdenberg, A.M., Molecular genetics of migraine (2009) Hum Genet, 126, pp. 115-132. , CrossRef Medline
  • Eikermann-Haerter, K., Yuzawa, I., Qin, T., Wang, Y., Baek, K., Kim, Y.R., Hoffmann, U., Ayata, C., Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice (2011) J Neurosci, 31, pp. 5755-5763. , CrossRef Medline
  • Fedchyshyn, M.J., Wang, L.Y., Developmental transformation of the release modality at the calyx of Held synapse (2005) J Neurosci, 25, pp. 4131-4140. , CrossRef Medline
  • Fioravante, D., Chu, Y., Myoga, M.H., Leitges, M., Regehr, W.G., Calciumdependent isoforms of protein kinase C mediate posttetanic potentiation at the calyx of Held (2011) Neuron, 70, pp. 1005-1019. , CrossRef Medline
  • Forsythe, I.D., Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro (1994) J Physiol, 479, pp. 381-387. , Medline
  • Forsythe, I.D., Tsujimoto, T., Barnes-Davies, M., Cuttle, M.F., Takahashi, T., Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse (1998) Neuron, 20, pp. 797-807. , CrossRef Medline
  • Gao, Z., Todorov, B., Barrett, C.F., van Dorp, S., Ferrari, M.D., van den Maagdenberg, A.M., de Zeeuw, C.I., Hoebeek, F.E., Cerebellar ataxia by enhanced CaV2.1 currents is alleviated by Ca 2-dependent K-channel activators in Cacna1a S218L mutant mice (2012) J Neurosci, 32, pp. 15533-15546. , CrossRef Medline
  • Giugovaz-Tropper, B., González-Inchauspe, C., Di Guilmi, M.N., Urbano, F.J., Forsythe, I.D., Uchitel, O.D., P/Q-type calcium channel ablation in a mice glycinergic synapse mediated by multiple types of Ca 2 channels alters transmitter release and short term plasticity (2011) Neuroscience, 192, pp. 219-230. , CrossRef Medline
  • Grande, G., Wang, L.Y., Morphological and functional continuum underlying heterogeneity in the spiking fidelity at the calyx of Held synapse in vitro (2011) J Neurosci, 31, pp. 13386-13399. , CrossRef Medline
  • Grynkiewicz, G., Poenie, M., Tsien, R.Y., A new generation of Ca 2 indicators with greatly improved fluorescence properties (1985) J Biol Chem, 260, pp. 3440-3450. , Medline
  • Guinan Jr., J.J., Li, R.Y., Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat (1990) Hear Res, 49, pp. 321-334. , CrossRef Medline
  • Habets, R.L., Borst, J.G.G., Post-tetanic potentiation in the rat calyx of Held synapse (2005) J Physiol, 564, pp. 173-187. , CrossRef Medline
  • Hermann, J., Pecka, M., von Gersdorff, H., Grothe, B., Klug, A., Synaptic transmission at the calyx of Held under in vivo like activity levels (2007) J Neurophysiol, 98, pp. 807-820. , CrossRef Medline
  • Hermann, J., Grothe, B., Klug, A., Modeling short-term synaptic plasticity at the calyx of Held using in vivo-like stimulation patterns (2009) J Neurophysiol, 101, pp. 20-30. , CrossRef Medline
  • Inchauspe, C.G., Martini, F.J., Forsythe, I.D., Uchitel, O.D., Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of Held presynaptic terminal (2004) J Neurosci, 24, pp. 10379-10383. , CrossRef Medline
  • Inchauspe, C.G., Forsythe, I.D., Uchitel, O.D., Changes in synaptic transmission properties due to the expression of N-type calcium channels at the calyx of Held synapse of mice lacking P/Q-type calcium channels (2007) J Physiol, 584, pp. 835-851. , CrossRef Medline
  • Inchauspe, C.G., Urbano, F.J., Di Guilmi, M.N., Forsythe, I.D., Ferrari, M.D., van den Maagdenberg, A.M., Uchitel, O.D., Gain of function in FHM-1 Ca(V)2.1 knock-in mice is related to the shape of the action potential (2010) J Neurophysiol, 104, pp. 291-299. , CrossRef Medline
  • Inchauspe, C.G., Urbano, F.J., Di Guilmi, M.N., Ferrari, M.D., van den Maagdenberg, A.M., Forsythe, I.D., Uchitel, O.D., Presynaptic CaV2.1 calcium channels carrying familial hemiplegic migraine mutation R192Q allow faster recovery from synaptic depression in mouse calyx of Held (2012) J Neurophysiol, 108, pp. 2967-2976. , CrossRef Medline
  • Iwasaki, S., Takahashi, T., Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem (1998) J Physiol, 509, pp. 419-423. , CrossRef Medline
  • Kaja, S., Van de Ven, R.C., Broos, L.A., Frants, R.R., Ferrari, M.D., Van den Maagdenberg, A.M., Plomp, J.J., Severe and progressive neurotransmitter release aberrations in familial hemiplegic migraine type 1 Cacna1a S218L knock-in mice (2010) J Neurophysiol, 104, pp. 1445-1455. , CrossRef Medline
  • Kochubey, O., Schneggenburger, R., Ca 2 uncaging in nerve terminals (2010) Optical Imaging In Neuroscience: A Laboratory Manual, pp. 151-160. , Konnerth A, Helmchen F, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
  • Korogod, N., Lou, X., Schneggenburger, R., Presynaptic Ca 2 requirements and developmental regulation of posttetanic potentiation at the calyx of Held (2005) J Neurosci, 25, pp. 5127-5137. , CrossRef Medline
  • Korogod, N., Lou, X., Schneggenburger, R., Posttetanic potentiation critically depends on an enhanced Ca 2 sensitivity of vesicle fusion mediated by presynaptic PKC (2007) Proc Natl Acad Sci U S A, 104, pp. 15923-15928. , CrossRef Medline
  • Kors, E.E., Terwindt, G.M., Vermeulen, F.L., Fitzsimons, R.B., Jardine, P.E., Heywood, P., Love, S., Ferrari, M.D., Delayed cerebral edema and fatal coma after minor head trauma: Role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine (2001) Ann Neurol, 49, pp. 753-760. , CrossRef Medline
  • Lauritzen, M., Pathophysiology of the migraine aura. The spreading depression theory (1994) Brain, 117, pp. 199-210. , CrossRef Medline
  • Lee, J.S., Kim, M.H., Ho, W.K., Lee, S.H., Presynaptic release probability and readily releasable pool size are regulated by two independent mechanisms during posttetanic potentiation at the calyx of Held synapse (2008) J Neurosci, 28, pp. 7945-7953. , CrossRef Medline
  • Lee, J.S., Ho, W.K., Lee, S.H., Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool (2012) Proc Natl Acad Sci USA109, pp. E765-E774. , CrossRefMedline
  • Lin, K.H., Erazo-Fischer, E., Taschenberger, H., Similar intracellular Ca 2 requirements for inactivation and facilitation of voltage-gated Ca 2 channels in a glutamatergic mammalian nerve terminal (2012) J Neurosci, 32, pp. 1261-1272. , CrossRef Medline
  • Lipstein, N., Sakaba, T., Cooper, B.H., Lin, K.H., Strenzke, N., Ashery, U., Rhee, J.S., Brose, N., Dynamic control of synaptic vesicle replenishment and short-term plasticity by Ca 2-calmodulinMunc13-1 signaling (2013) Neuron, 79, pp. 82-96. , CrossRef Medline
  • Lorteije, J.A., Rusu, S.I., Kushmerick, C., Borst, J.G.G., Reliability and precision of the mouse calyx of Held synapse (2009) J Neurosci, 29, pp. 13770-13784. , CrossRef Medline
  • Lou, X., Scheuss, V., Schneggenburger, R., Allosteric modulation of the presynaptic Ca 2 sensor for vesicle fusion (2005) Nature, 435, pp. 497-501. , CrossRef Medline
  • Muller, M., Felmy, F., Schwaller, B., Schneggenburger, R., Parvalbumin is a mobile presynaptic Ca 2 buffer in the calyx of Held that accelerates the decay of Ca 2 and short-term facilitation (2007) J Neurosci, 27, pp. 2261-2271. , CrossRef Medline
  • Neher, E., Sakaba, T., Multiple roles of calcium ions in the regulation of neurotransmitter release (2008) Neuron, 59, pp. 861-872. , CrossRef Medline
  • Ophoff, R.A., Terwindt, G.M., Vergouwe, M.N., van Eijk, R., Oefner, P.J., Hoffman, S.M., Lamerdin, J.E., Frants, R.R., Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca 2 channel gene CACNL1A4 (1996) Cell, 87, pp. 543-552. , CrossRef Medline
  • Pang, Z.P., Bacaj, T., Yang, X., Zhou, P., Xu, W., Sudhof, T.C., Doc2 supports spontaneous synaptic transmission by a Ca 2-independent mechanism (2011) Neuron, 70, pp. 244-251. , CrossRef Medline
  • Pietrobon, D., Calcium channels and migraine (2013) Biochim Biophys Acta, 1828, pp. 1655-1665. , CrossRef Medline
  • Rodríguez-Contreras, A., van Hoeve, J.S., Habets, R.L., Locher, H., Borst, J.G.G., Dynamic development of the calyx of Held synapse (2008) Proc Natl Acad Sci U S A, 105, pp. 5603-5608. , CrossRef Medline
  • Sakaba, T., Neher, E., Calmodulin mediates rapid recruitment of fastreleasing synaptic vesicles at a calyx-type synapse (2001) Neuron, 32, pp. 1119-1131. , CrossRef Medline
  • Schneggenburger, R., Meyer, A.C., Neher, E., Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse (1999) Neuron, 23, pp. 399-409. , CrossRef Medline
  • Shu, Y., Hasenstaub, A., McCormick, D.A., Turning on and off recurrent balanced cortical activity (2003) Nature, 423, pp. 288-293. , CrossRef Medline
  • Somjen, G.G., Ion regulation in the brain: Implications for pathophysiology (2002) Neuroscientist, 8, pp. 254-267. , Medline
  • Stam, A.H., Luijckx, G.J., Poll-Thé, B.T., Ginjaar, I.B., Frants, R.R., Haan, J., Ferrari, M.D., van den Maagdenberg, A.M., Early seizures and cerebral oedema after trivial head trauma associated with the CACNA1A S218L mutation (2009) J Neurol Neurosurg Psychiatry, 80, pp. 1125-1129. , CrossRef Medline
  • Sun, J., Pang, Z.P., Qin, D., Fahim, A.T., Adachi, R., Sudhof, T.C., A dual-Ca 2-sensor model for neurotransmitter release in a central synapse (2007) Nature, 450, pp. 676-682. , CrossRef Medline
  • Tan, M.L., Borst, J.G.G., Comparison of responses of neurons in the mouse inferior colliculus to current injections, tones of different durations, and sinusoidal amplitude-modulated tones (2007) J Neurophysiol, 98, pp. 454-466. , CrossRef Medline
  • Thomsen, L.L., Eriksen, M.K., Roemer, S.F., Andersen, I., Olesen, J., Russell, M.B., A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria (2002) Brain, 125, pp. 1379-1391. , CrossRef Medline
  • Tottene, A., Pivotto, F., Fellin, T., Cesetti, T., van den Maagdenberg, A.M., Pietrobon, D., 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 (2005) J Biol Chem, 280, pp. 17678-17686. , CrossRef Medline
  • Tottene, A., Conti, R., Fabbro, A., Vecchia, D., Shapovalova, M., Santello, M., van den Maagdenberg, A.M., Pietrobon, D., Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice (2009) Neuron, 61, pp. 762-773. , CrossRef Medline
  • Urbano, F.J., Piedras-Rentería, E.S., Jun, K., Shin, H.S., Uchitel, O.D., Tsien, R.W., Altered properties of quantal neurotransmitter release at endplates of mice lacking P/Q-type Ca 2 channels (2003) Proc Natl Acad Sci U S A, 100, pp. 3491-3496. , CrossRef Medline
  • van den Maagdenberg, A.M., Pietrobon, D., Pizzorusso, T., Kaja, S., Broos, L.A., Cesetti, T., van de Ven, R.C., Ferrari, M.D., A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression (2004) Neuron, 41, pp. 701-710. , CrossRef Medline
  • van den Maagdenberg, A.M., Pizzorusso, T., Kaja, S., Terpolilli, N., Shapovalova, M., Hoebeek, F.E., Barrett, C.F., Ferrari, M.D., High cortical spreading de-pression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice (2010) Ann Neurol, 67, pp. 85-98. , CrossRef Medline
  • Varela, J.A., Sen, K., Gibson, J., Fost, J., Abbott, L.F., Nelson, S.B., A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex (1997) J Neurosci, 17, pp. 7926-7940. , Medline
  • Wang, L.Y., Kaczmarek, L.K., High-frequency firing helps replenish the readily releasable pool of synaptic vesicles (1998) Nature, 394, pp. 384-388. , CrossRef Medline
  • Wang, T., Rusu, S.I., Hruskova, B., Turecek, R., Borst, J.G.G., Modulation of synaptic depression of the calyx of Held synapse by GABAB receptors and spontaneous activity (2013) J Physiol, 591, pp. 4877-4894. , CrossRef Medline
  • Xu, J., Pang, Z.P., Shin, O.H., Sudhof, T.C., Synaptotagmin-1 functions as a Ca 2 sensor for spontaneous release (2009) Nat Neurosci, 12, pp. 759-766. , CrossRef Medline

Citas:

---------- APA ----------
Di Guilmi, M.N., Wang, T., Inchauspe, C.G., Forsythe, I.D., Ferrari, M.D., Van Der Maagdenberg, A.M.J.M., Borst, J.G.G.,..., Uchitel, O.D. (2014) . Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i. Journal of Neuroscience, 34(21), 7047-7058.
http://dx.doi.org/10.1523/JNEUROSCI.2526-13.2014
---------- CHICAGO ----------
Di Guilmi, M.N., Wang, T., Inchauspe, C.G., Forsythe, I.D., Ferrari, M.D., Van Der Maagdenberg, A.M.J.M., et al. "Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i" . Journal of Neuroscience 34, no. 21 (2014) : 7047-7058.
http://dx.doi.org/10.1523/JNEUROSCI.2526-13.2014
---------- MLA ----------
Di Guilmi, M.N., Wang, T., Inchauspe, C.G., Forsythe, I.D., Ferrari, M.D., Van Der Maagdenberg, A.M.J.M., et al. "Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i" . Journal of Neuroscience, vol. 34, no. 21, 2014, pp. 7047-7058.
http://dx.doi.org/10.1523/JNEUROSCI.2526-13.2014
---------- VANCOUVER ----------
Di Guilmi, M.N., Wang, T., Inchauspe, C.G., Forsythe, I.D., Ferrari, M.D., Van Der Maagdenberg, A.M.J.M., et al. Synaptic gain-of-function effects of mutant Cav2.1 channels in a mouse model of familial hemiplegic migraine are due to increased basal [Ca2+]i. J. Neurosci. 2014;34(21):7047-7058.
http://dx.doi.org/10.1523/JNEUROSCI.2526-13.2014