Abstract
Junctophilins (JPs) contribute to the formation of junctional membrane complexes between the plasma membrane and the endoplasmic/sarcoplasmic reticulum, and provide a structural platform for channel communication during excitation–contraction coupling in muscle cells. In the brain, two neuronal JP subtypes are widely expressed in neurons. Recent studies have defined the essential role of neural JPs in the communication between cell-surface and intracellular channels, which modulates the excitability and synaptic plasticity of neurons in the cerebellum and hippocampus.
Similar content being viewed by others
References
Pozzan T, Rizzuto R, Volpe P, Meldolesi J (1994) Molecular and cellular physiology of intracellular calcium stores. Physiol Rev 74:595–636
Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13–26
Flucher BE (1992) Structural-analysis of muscle development—transverse tubules, sarcoplasmic-reticulum, and the triad. Dev Biol 154:245–260
Tanabe T, Beam KG, Powell JA, Numa S (1988) Restoration of excitation–contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary-DNA. Nature 336:134–139
Takeshima H, Iino M, Takekura H, Nishi M, Kuno J, Minowa O et al (1994) Excitation–contraction uncoupling and muscular degeneration in mice lacking functional skeletal-muscle ryanodine-receptor gene. Nature 369:556–559
Endo M (1985) Calcium release from sarcoplasmic-reticulum. Curr Top Membr Transp 25:181–230
Takekura H, Takeshima H, Nishimura S, Takahashi M, Tanabe T, Flockerzi V et al (1995) Coexpression in Cho cells of 2 muscle proteins involved in excitation–contraction coupling. J Muscle Res Cell Motil 16:465–480
Suda N, Franzius D, Fleig A, Nishimura S, Bodding M, Hoth M et al (1997) Ca2+-induced Ca2+ release in Chinese hamster ovary (CHO) cells co-expressing dihydropyridine and ryanodine receptors. J Gen Physiol 109:619–631
Franzini-Armstrong C, Pinconraymond M, Rieger F (1991) Muscle-fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings. Dev Biol 146:364–376
Ikemoto T, Komazaki S, Takeshima H, Nishi M, Noda T, Iino M et al (1997) Functional and morphological features of skeletal muscle from mutant mice lacking both type 1 and type 3 ryanodine receptors. J Physiol-Lond 501:305–312
Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6:11–22
Ito K, Komazaki S, Sasamoto K, Yoshida M, Nishi M, Kitamura K et al (2001) Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J Cell Biol 154:1059–1067
Nishi M, Sakagami H, Komazaki S, Kondo H, Takeshima H (2003) Coexpression of junctophilin type 3 and type 4 in brain. Mol Brain Res 118:102–110
Nishi M, Hashimoto K, Kuriyama K, Komazaki S, Kano M, Shibata S et al (2002) Motor discoordination in mutant mice lacking junctophilin type 3. Biochem Biophys Res Commun 292:318–324
Moriguchi S, Nishi M, Komazaki S, Sakagami H, Miyazaki T, Masumiya H et al (2006) Functional uncoupling between Ca2+ release and afterhyperpolarization in mutant hippocampal neurons lacking junctophilins. Proc Natl Acad Sci USA 103:10811–10816
Kakizawa S, Kishimoto Y, Hashimoto K, Miyazaki T, Furutani K, Shimizu H et al (2007) Junctophilin-mediated channel crosstalk essential for cerebellar synaptic plasticity. EMBO J 26:1924–1933
Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje-cells. Proc Natl Acad Sci USA 87:2662–2665
Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78:272–303
Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang HP et al (1998) Phospholipase C beta 4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95:15724–15729
Kakizawa S, Yamasaki M, Watanabe M, Kano M (2000) Critical period for activity-dependent synapse elimination in developing cerebellum. J Neurosci 20:4954–4961
Kakizawa S, Yamada K, Iino M, Watanabe M, Kano M (2003) Effects of insulin-like growth factor I on climbing fibre synapse elimination during cerebellar development. Eur J Neurosci 17:545–554
Kakizawa S, Miyazaki T, Yanagihara D, Iino M, Watanabe M, Kano M (2005) Maintenance of presynaptic function by AMPA receptor-mediated excitatory postsynaptic activity in adult brain. Proc Natl Acad Sci USA 102:19180–19185
Hashimoto K, Kano M (2005) Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci Res 53:221–228
Schmolesky MT, Weber JT, De Zeeuw CI, Hansel C (2002) The making of a complex spike: ionic composition and plasticity. Ann NY Acad Sci 978(1):359–390
Pedarzani P, Mosbacher J, Rivard A, Cingolani LA, Oliver D, Stocker M et al (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
Knaus HG, Schwarzer C, Koch ROA, Eberhart A, Kaczorowski GJ, Glossmann H et al (1996) Distribution of high-conductance Ca2+-activated K+ channels in rat brain: targeting to axons and nerve terminals. J Neurosc 16:955–963
Womack MD, Khodakhah K (2002) Characterization of large conductance Ca2+-activated K+ channels in cerebellar Purkinje neurons. Eur J Neurosci 16:1214–1222
Edgerton JR, Reinhart PH (2003) Distinct contributions of small and large conductance Ca2+-activated K+ channels to rat Purkinje neuron function. J Physiol-Lond 548:53–69
Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J et al (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273:1709–1714
Sailer CA, Kaufmann WA, Marksteiner J, Knaus HG (2004) Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Mol Cell Neurosci 26:458–469
Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J et al (2004) Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24:5301–5306
Grunnet M, Jensen BS, Olesen SP, Klaerke DA (2001) Apamin interacts with all subtypes of cloned small-conductance Ca2+-activated K+ channels. Pflugers Archiv European Journal of Physiology 441:544–550
Linden DJ, Connor JA (1995) Long-term synaptic depression. Annu Rev Neurosci 18:319–357
Weber JT, De Zeeuw CI, Linden DJ, Hansel C (2003) Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc Natl Acad Sci USA 100:2878–2883
Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691–700
Ikeda A, Miyazaki T, Kakizawa S, Okuno Y, Tsuchiya S, Myomoto A et al (2007) Abnormal features in mutant cerebellar Purkinje cells lacking junctophilins. Biochem Biophys Res Commun 363:835–839
Verkhratsky A (2002) The endoplasmic reticulum and neuronal calcium signalling. Cell Calcium 32:393–404
Rose CR, Konnerth A (2001) Stores not just for storage: intracellular calcium release and synaptic plasticity. Neuron 31:519–522
Bardo S, Cavazzini MG, Emptage N (2006) The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol Sci 27:78–84
Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4, 5-trisphosphate in Purkinje cell dendrites. Nature 396:753–756
Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines. Nature 396:757–760
Kano M, Garaschuk O, Verkhratsky A, Konnerth A (1995) Ryanodine receptor-mediated intracellular calcium-release in rat cerebellar Purkinje neurons. J Physiol-Lond 487:1–16
Garaschuk O, Yaari Y, Konnerth A (1997) Release and sequestration of calcium by ryanodine-sensitive stores in rat hippocampal neurones. J Physiol-Lond 502:13–30
Llano I, Dipolo R, Marty A (1994) Calcium-induced calcium-release in cerebellar Purkinje-cells. Neuron 12:663–673
Verkhratsky A (2005) Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201–279
Furuichi T, Furutama D, Hakamata Y, Nakai J, Takeshima H, Mikoshiba K (1994) Multiple types of ryanodine receptor Ca2+ release channels are differentially expressed in rabbit brain. J Neurosci 14:4794–4805
Furuichi T, Simonchazottes D, Fujino I, Yamada N, Hasegawa M, Miyawaki A et al (1993) Widespread expression of inositol 1,4,5-trisphosphate receptor type-1 gene (Insp3r1) in the mouse central-nervous-system. Recept Channels 1:11–24
Inoue T, Kato K, Kohda K, Mikoshiba K (1998) Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J Neurosci 18:5366–5373
Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI et al (2000) Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28:233–244
Furutani K, Okubo Y, Kakizawa S, Iino M (2006) Postsynaptic inositol 1,4,5-trisphosphate signaling maintains presynaptic function of parallel fiber-Purkinje cell synapses via BDNF. Proc Natl Acad Sci USA 103:8528–8533
Kohda K, Inoue T, Mikoshiba K (1995) Ca2+ release from Ca2+ stores, particularly from ryanodine-sensitive Ca2+ stores, is required for the induction of Ltd in cultured cerebellar Purkinje-cells. J Neurophysiol 74:2184–2188
Iino M (1990) Biphasic Ca2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth-muscle cells of the guinea-pig taenia ceci. J Gen Physiol 95:1103–1122
Bezprozvanny I, Watras J, Ehrlich BE (1991) Bell-shaped calcium-response curves of Ins(1,4,5)P3-gated and calcium-gated channels from endoplasmic-reticulum of cerebellum. Nature 351:751–754
Wang SSH, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266–1273
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kakizawa, S., Moriguchi, S., Ikeda, A. et al. Functional Crosstalk Between Cell-Surface and Intracellular Channels Mediated by Junctophilins Essential for Neuronal Functions. Cerebellum 7, 385–391 (2008). https://doi.org/10.1007/s12311-008-0040-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12311-008-0040-1