Biochemical properties and subcellular distribution of the neuronal class E calcium channel α1 subunit

Journal of Neuroscience

Volumn 15, Issue 10, 1995, Pages 6419-6432

  Yokoyama, Charles T ^a   Westenbroek, Ruth E ^a   Hell, Johannes W ^a   Soong, Tuck Wah ^b   Snutch, Terry P ^b   Catterall, William A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

calcium channel; immunocytochemistry; ion channel; peptide toxin; phosphorylation; Purkinje cell

Indexed keywords

BRAIN PROTEIN; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; DIHYDROPYRIDINE DERIVATIVE; IODINE 125; ISRADIPINE; OMEGA CONOTOXIN GVIA; OMEGA CONOTOXIN MVIIC; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C; TOXIN; TRITIUM;

ALPHA CHAIN; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

EID: 0028829634     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-10-06419.1995     Document Type: Article

References (80)

1. Ahlijanian MK, Westenbroek RE, Catterall WA (1990) Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina. Neuron 4:819-832.
2. Armstrong DL, Rossier MF, Shcherbatko AD, White RE (1991) Enzymatic gating of voltage-gated calcium channels. Ann NY Acad Sci 635:26-34.
3. Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181-186.
4. Bean BP (1989) Classes of calcium channels in vertebrate cells. Annu Rev Physiol 51:367-384.
5. Birnbaumer L, Campbell KP, Catterall WA, Harpold MM, Hofmann F, Home WA, Mori Y, Schwartz A, Snutch TP, Tanabe T, Tsien RW (1994) The naming of voltage-gated calcium channels. Neuron 13: 505-506.
6. 1E calcium channels display permeation characteristics similar to low voltage activated channels. Soc Neurosci Abstr 20:70.
7. 2+/calmodulin-dependent protein kinase II using the baculovirus expression system. Biochem Biophys Res Commun 173:578-584.
8. Catterall WA (1994) Molecular properties of a superfamily of plasma membrane cation channels. Curr Opin Cell Biol 6:607-615.
9. Coppola T, Waldmann R, Borsotto M, Heurteaux C, Romey G, Mattei M-G, Lazdunski M (1994) Molecular cloning of a murine N-type channel α1 subunit: evidence for isoforms, brain distribution, and chromosomal localization. FEBS Lett 338:1-5.
10. Dolphin AC (1990) G protein modulation of calcium currents in neurons. Annu Rev Physiol 52:243-255.
11. Dubel SJ, Starr TVB, Hell J, Ahlijanian MK, Enyeart JJ, Catterall WA, Snutch TP (1992) Molecular cloning of the α1 subunit of an ω-conotoxin-sensitive calcium channel. Proc Natl Acad Sci USA 89:5058-5062.
12. Eilers J-K, Augustine GJ, Konnerth A (1994) Subthreshold synaptic calcium signaling in dendrites and spines of cerebellar Purkinje neurons. Nature 373:155-158.
13. Ellinor PT, Zhang J-F, Randall AD, Zhou M, Schwarz TL, Tsien RW, Home WA (1993) Functional expression of a rapidly inactivating neuronal calcium channel. Nature 363:455-458.
14. Ellisman MH, Deerinck TJ, Ouyang Y, Beck CF, Tanksley SJ, Walton PD, Airey JA, Sutko JL (1990) Identification and localization of ryanodine binding proteins in the avian central nervous system. Neuron 5:135-146.
15. Forti L, Tottene A, Moretti A, Pietrobon D (1994) Three novel types of voltage-dependent calcium channels in rat cerebellar neurons. J Neurosci 14:5243-5256.
16. Fortier L-P, Tremblay J-P, Rafrafi J, Hawkes R (1991) A monoclonal antibody to conotoxin reveals the distribution of a subset of calcium channels in the rat cerebellar cortex. Mol Brain Res 9:209-215.
17. Fujita Y, Mynlieff M, Dirksen RT, Kim MS, Niidome T, Nakai J, Freidrich T, Iwabe N, Miyata T, Furuichi T, Furutama D, Mikoshiba K, Mori Y, Beam KG (1993) Primary structure and functional expression of the ω-conotoxin-sensitive N-type calcium channel from rabbit brain. Neuron 10:585-598.
18. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, Gilbert MM, Snutch TP, Catterall WA (1993a) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel α1 subunits. J Cell Biol 123:949-961.
19. Hell JW, Yokoyama CT, Wong ST, Warner C, Snutch TP, Catterall WA (1993b) Differential phosphorylation of two size forms of the neuronal class C L-type channel. J Biol Chem 268:19451-19457.
20. Hell JW, Appleyard SM, Yokoyama CT, Warner C, Catterall WA (1994) Differential phosphorylation of two size forms of the N-type calcium channel α1 subunit which have different COOH termini. J Biol Chem 269:7390-7396.
21. Hell JW, Westenbroek RE, Elliott EM, Catterall WA (1995a) Differential phosphorylation, localization, and function of distinct α1 sybunits of neuronal calcium channels. Ann NY Acad Sci, in press.
22. Hell JW, Yokoyama CT, Breeze LJ, Chavkin C, Catterall WA (1995b) Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP-dependent protein kinase in hippocampal neurons. EMBO J, in press.
23. 2+ channels in evoked release of norepinephrine from sympathetic neurons. Science 239:57-60.
24. 2+ channel diversity. Annu Rev Neurosci 17:399-418.
25. 2+-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 12:3804-3817.
26. Hui A, Ellinor PT, Krizanova O, Wang J-J, Diebold RJ, Schwartz A (1991) Molecular cloning of multiple subtypes of a novel rat brain isoform of the α1 subunit of the voltage-dependent calcium channel. Neuron 7:35-44.
27. Hui SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
28. Isom LL, DeJongh KS, Catterall WA (1994) Auxiliary subunits of voltage-gated ion channels. Neuron 12:1183-1194.
29. Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol (Lond) 324:113-134.
30. Kaczmarek LK, Jennings KR, Strumwasser F, Nairn AC, Walter U, Wilson FD, Greengard P (1980) Microinjection of catalytic subunit of cAMP-dependent protein kinase enhances calcium action potentials of bag cell neurons in cell culture. Proc Natl Acad Sci USA 77: 7487-7491.
31. Konnerth A, Dreesen J, Augustine GJ (1992) Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells. Proc Natl Acad Sci USA 89:7051-7055.
32. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680-685.
33. Llinas R, Sugimori M (1979) Calcium conductances in Purkinje cell dendrites: their role in development and integration. Prog Brain Res 51:323-334.
34. Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
35. Luebke JI, Dunlap K, Turner TJ (1993) Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron 11:895-902.
36. 1E calcium channel splice variants. Soc Neurosci Abstr 20:69.
37. McCleskey EW (1994) Calcium channels: cellular roles and molecular mechanisms. Curr Opin Neurobiol 4:304-312.
38. McLean IW, Nakane P (1974) Periodate-lysine-paraformaldehyde fixative for immunoelectron microscopy. J Histochem Cytochem 22: 1077-1083.
39. 2+ current modulated by cGMP-dependent protein kinase. Nature 369:336-339.
40. Merrifield RB (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J Am Chem Soc 85:2149-2154.
41. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, Adams ME (1992) P-Type calcium channels blocked by the spider toxin ω-AgaIVA. Nature 355:827-829.
42. Morgan JI, Curran T (1986) Role of ion flux in the control of c-fos expression. Nature 322:552-555.
43. Mori Y, Friedrich T, Kim MS, Mikami A, Nakai J, Ruth P, Bosse E, Hofmann F, Flockerzi V, Furuichi T, Mikoshiba K, Imoto K, Tanabe T, Numa S (1991) Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature 350:398-402.
44. + channel reconstituted into phospholipid vesicles by protein kinase C. J Biol Chem 267:16129-16134.
45. Murphy TH, Worley PF, Baraban JM (1991) L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron 7:625-635.
46. Niidome T, Kim M, Friedrich T, Mori Y (1992) Molecular cloning and characterization of a novel calcium channel from rat brain. FEBS Lett 308:7-13.
47. Orth DN (1979) Methods of hormone radioimmunoassay, pp 245-284. New York: Academic.
48. Randall AD, Tsien RW (1995) Pharmacological dissection of multiple types of calcium channel currents in rat cerebellar granule neurons. J Neurosci 15:2995-3012.
49. Rotman EI, DeJongh KS, Florio V, Lai Y, Catterall WA (1992) Specific phosphorylation of a COOH-terminal site on the full-lengh form of the α1 subunit of the skeletal muscle calcium channel by cAMP-dependent protein kinase. J Biol Chem 267:16100-16105.
50. Sather WA, Tanabe T, Zhang J-F, Mori Y, Adams ME, Tsien RW (1993) Distinctive biophysical and pharmacological properties of class A (B1) calcium channel α1 subunits. Neuron 11:291-303.
51. 2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature 364:240-243.
52. 2+ channels: diversity of form and function. Curr Opin Neurobiol 2:247-253.
53. Snutch TP, Leonard JP, Gilbert MM, Lester HA, Davidson N (1990) Rat brain expresses a heterogeneous family of calcium channels. Proc Natl Acad Sci USA 87:3391-3395.
54. Snutch TP, Tomlinson WJ, Leonard JP, Gilbert MM (1991) Distinct calcium channels are generated by alternative splicing and are differentially expressed in the mammalian CNS. Neuron 7:45-57.
55. Soong TW, Stea A, Hodson CD, Dubel SJ, Vincent SR, Snutch TP (1993) Structure and functional expression of a member of the low voltage-activated calcium channel family. Science 260:1133-1136.
56. Starr TVB, Prystay W, Snutch TP (1991) Primary structure of a calcium channel that is highly expressed in the rat cerebellum. Proc Natl Acad Sci USA 88:5621-5625.
57. 1A calcium channel reflect similarities to neuronal Q- and P-type channels. Proc Natl Acad Sci USA 91:10576-10580.
58. 1B calcium channels. Soc Neurosci Abstr 20:1468.
59. 2+ channels. Proc Natl Acad Sci USA 87:9108-9112.
60. 2+ channels by protein kinase C in rat central and peripheral neurons: disruption of G-protein mediated inhibition. Neuron 11:305-320.
61. Takahashi T, Momiyama A (1993) Different types of calcium channels mediate central synaptic transmission. Nature 366:156-158.
62. Tank DW, Sugimori M, Connor JA, Llinas RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242:773-777.
63. Trautwein W, Hescheler J (1990) Regulation of cardiac L-type calcium current by phosphorylation and G-proteins. Annu Rev Physiol 52: 257-274.
64. 2+ channels. Trends Pharmacol Sci 12:349-352.
65. Turner TJ, Adams ME, Dunlap K (1992) Calcium channels coupled to glutamate release identified by ω-Aga-IVA. Science 258:310-313.
66. 2+ channel types coexist to regulate synaptosomal neurotransmitter release. Proc Natl Acad Sci USA 90:9518-9522.
67. Usowicz MM, Sugimori M, Cherksey B, Llinas R (1992) P-Type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron 9:1185-1199.
68. Wakamori M, Niidome T, Mori Y (1993) Functional expression of a novel type of calcium channel from cDNA. Soc Neurosci Abstr 19: 11.
69. Walton PD, Airey JA, Sutko JL, Beck CF, Mignery GA, Sudhof TC, Deerinck TJ, Ellisman MH (1991) Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J Cell Biol 113:1145-1157.
70. 2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347:281-284.
71. Westenbroek RE, Hell JW, Warner C, Dubel SJ, Snutch TP, Catterall WA (1992) Biochemical properties and subcellular distribution of an N-type calcium channel α1 subunit. Neuron 9:1099-1115.
72. Westenbroek RE, Hell JW, Sakurai T, Snutch TP, Catterall WA (1993) Immunocytochemical localization of class A calcium channels in adult rat brain. Soc Neurosci Abstr 19:1334.
73. 1A subunits of brain calcium channels. J Neurosci 15:6403-6418.
74. 2+ channels in supporting hippocampal synaptic transmission. Science 264:107-111.
75. Williams ME, Feldman DH, McCue AF, Brenner R, Velicelebi G, Ellis SB, Harpold MM (1992a) Structure and functional expression of α1, α2, and β subunits of a novel human neuronal calcium channel subtype. Neuron 8:71-84.
76. Williams ME, Brust PF, Feldman DH, Patthi S, Simerson S, Maroufi A, McCue AF, Velicelebi G, Ellis SB, Harpold MM (1992b) Structure and functional expression of an ω-conotoxin-sensitive human N-type calcium channel. Science 257:389-395.
77. 1E calcium channel subtypes. J Biol Chem 269:22347-22357.
78. Woodgett JR, Hunter T (1987) Isolation and characterization of two distinct forms of protein kinase C. J Biol Chem 262:4836-4843.
79. Yang J, Tsien RW (1993) Enhancement of N- and L-type calcium channel currents by protein kinase C in frog sympathetic neurons. Neuron 10:127-136.
80. 2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology 32:1075-1088.