Alternative splicing of a short cassette exon in α(1B) generates functionally distinct N-type calcium channels in central and peripheral neurons

Journal of Neuroscience

Volumn 19, Issue 13, 1999, Pages 5322-5331

  Lin, Zhixin ^a   Lin, Yingxin ^a   Schorge, Stephanie ^a   Pan, Jennifer Qian ^a   Beierlein, Michael ^a   Lipscombe, Diane ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Calcium channel 1 subunits; Genomic analysis; N type calcium channel; P Q type calcium channel; Regulated alternative splicing; S3 S4 linker

Indexed keywords

CALCIUM; CALCIUM CHANNEL; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXON; GENE CASSETTE; NERVE POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; OOCYTE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SITE DIRECTED MUTAGENESIS; SYNAPSE; XENOPUS;

EID: 0033169067     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-13-05322.1999     Document Type: Article

References (63)

1. Augustine GJ, Neher E (1992) Calcium requirements for secretion in bovine chromaffin cells. J Physiol (Lond) 450:247-271.
2. Barry EL, Gesek FA, Froehner SC, Friedman PA (1995) Multiple calcium channel transcripts in rat osteosarcoma cells: selective activation of alpha 1D isoform by parathyroid hormone. Proc Natl Acad Sci USA 92:10914-10918.
3. Cestele S, Qu Y, Rogers JC, Rochat H, Scheuer T, Catterall WA (1998) Voltage sensor-trapping: enhanced activation of sodium channels by beta-scorpion toxin bound to the S3-S4 loop in domain II. Neuron 21:919-931.
4. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
5. Coppola T, Waldmann R, Borsotto M, Heurteaux C, Romey G, Mattei M-G, Lazdunski M (1994) Molecular cloning of a murine N-type calcium channel α1 subunit. Evidence for isoforms, brain distribution, and chromosomal localization. FEBS Lett 338:1-5.
6. Cota G, Nicola Siri L, Stefani EJ (1983) Calcium-channel gating in frog skeletal muscle membrane: effect of temperature. J Physiol (Lond) 338:395-412.
7. 1 subunit of an ω-conotoxin-sensitive calcium channel. Proc Natl Acad Sci USA 89:5058-5062.
8. 2+ channels in mammalian central neurons. Trends Neurosci 18:89-98.
9. Ellinor PT, Zhang J-F, Home WA, Tsien RW (1994) Structural determinants of the blockade of N-type calcium channels by a peptide neurotoxin. Nature 372:272-275.
10. Fujita Y, Mynlieff M, Dirksen RT, Kim M-S, Niidome T, Nakai J, Friedrich T, Iwabe N, Miyata T, Furuichi T, Furuichi T, Furutama D, Mikoshiba K, Mori Y, Beam KG (1993) Primary structure and functional expression of the ω-conotoxin-sensitive N-type channel from rabbit brain. Neuron 10:585-598.
11. Goldin AL, Sumikawa K (1992) Preparation of RNA for injection into Xenopus oocytes. Methods Enzymol 207:279-297.
12. Grabowski PJ (1998) Splicing regulation in neurons: tinkering with cell-specific control. Cell 92:709-712.
13. 1A-containing high-voltage activated calcium channels. Biophys J 76:1384-1400.
14. Heidelberger R, Heinemann C, Neher E, Matthews G (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513-515.
15. Hille B (1992) Ionic channels of excitable membranes. Sunderland, MA: Sinauer.
16. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
17. 2+ channels in evoked release of norepinephrine from sympathetic neurons. Science 239:57-61.
18. Hogan K, Gregg RG, Powers PA (1996) The structure of the gene encoding the human skeletal muscle alpha 1 subunit of the dihydropyridine-sensitive L-type calcium channel (CACNL1A3). Genomics 31:392-394.
19. Ihara Y, Yamada Y, Fujii Y, Gonoi T, Yano H, Yasuda K, Inagaki N, Seino Y, Seino S (1995) Molecular diversity and functional characterization of voltage-dependent calcium channels (CACN4) expressed in pancreatic beta-cells. Mol Endocrinol 9:121-130.
20. Jones SW, Marks TN (1989) Calcium currents in bullfrog sympathetic neurons. II. Inactivation. J Gen Physiol 94:169-182.
21. Kammermeier PJ, Jones SW (1997) High-voltage-activated calcium currents in neurons acutely isolated from the ventrobasal nucleus of the rat thalamus. J Neurophysiol 77:465-475.
22. Klockner U, Mikala G, Eisfeld J, Iles DE, Strobeck M, Mershon JL, Schwartz A, Varadi G (1997) Properties of three COOH-terminal splice variants of a human cardiac L-type Ca2+-channel alphal-subunit. Am J Physiol 272:H1372-1381.
23. Ligon B, Boyd 3rd AE, Dunlap K (1998) Class A calcium channel variants in pancreatic islets and their role in insulin secretion. J Biol Chem 273:13905-13911.
24. 2+ channel in rat sympathetic ganglia and brain. Neuron 18:153-166.
25. 1B-subunit can account for the expression of kinetically distinct variants of the N-type Ca channel in the nervous system of the rat. J Physiol (Lond) 504:156.
26. Llinas R, Sugimori M, Lin JW, Cherksey B (1989) Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci USA 86:1689-1693.
27. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
28. Mathur R, Zheng J, Van Y, Sigworth FJ (1997) Role of the S3-S4 linker in Shaker potassium channel activation. J Gen Physiol 109:191-199.
29. Miljanich GP, Ramachandran J (1995) Antagonists of neuronal calcium channels: structure, function, and therapeutic implications. Annu Rev Pharmacol Toxicol 35:707-734.
30. Mintz IM, Adams ME, Bean BP (1992) P-type calcium channels in rat central and peripheral neurons. Neuron 9:85-95.
31. Nakai J, Adams BA, Imoto K, Beam KG (1994) Critical roles of the S3 segment and S3-S4 linker of repeat I in activation of L-type calcium channels. Proc Natl Acad Sci USA 91:1014-1018.
32. 2+] at the mouth of a calcium channel. J Neurosci 17:6961-6973.
33. Olivera BM, Miljanich GP, Ramachandran J, Adams ME (1994) Calcium channel diversity and neurotransmitter release: the omega-conotoxins and omega-agatoxins. Annu Rev Biochem 63:823-867.
34. 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.
35. Perez-Reyes E, Weil XY, Castellano A, Birnbaumer L (1990) Molecular diversity of L-type calcium channels. Evidence for alternative splicing of the transcripts of three non-allelic genes. J Biol Chem 265:20430-20436.
36. 2+ channel currents in rat cerebellar granule neurons. J Neurosci 15:2995-3012.
37. Rogers JC, Qu Y, Tanada TN, Scheuer T, Catterall WA (1996) Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit. J Biol Chem 271:15950-15962.
38. Sather WA, Tanabe T, Zhang JF, Mori Y, Adams ME, Tsien RW (1993) Distinctive biophysical and pharmacological properties of class A (BI) calcium channel alpha 1 subunits. Neuron 11:291-303.
39. 1B subunits. Soc Neurosci Abstr 24:1327.
40. Sheng ZH, Rettig J, Takahashi M, Catterall WA (1994) Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13:1303-1313.
41. 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.
42. Soldatov NM (1994) Genomic structure of human L-type Ca2+ channel. Genomics 22:77-87.
43. Soldatov NM, Zuhlke RD, Bouron A, Reuter H (1997) Molecular structures involved in L-type calcium channel inactivation. Role of the carboxyl-terminal region encoded by exons 40-42 in alpha 1C subunit in the kinetics and Ca2+ dependence of inactivation. J Biol Chem 272:3560-3566.
44. Soong TW, Stea A, Hudson 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.
45. Starr TV, 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.
46. Stea A, Tomlinson WJ, Soong TW, Bourinet E, Dubel SJ, Vincent SR, Snutch TP (1994) Localization and functional properties of a rat brain alpha 1A calcium channel reflect similarities to neuronal Q-and P-type channels. Proc Natl Acad Sci USA 91:10576-10580.
47. 1A gene generates distinct P-or Q-type sensitivity to ω-agatoxin IVA. Soc Neurosci Abstr 24:21.
48. Swartz KJ, MacKinnon R (1997) Mapping the receptor site for hanatoxin, a gating modifier of voltage-dependent K+ channels. Neuron 18:675-682.
49. Takahashi T, Momiyama A (1993) Different types of calcium channels mediate central synaptic transmission. Nature 366:156-158.
50. Tang CY, Papazian DM (1997) Transfer of voltage independence from a rat olfactory channel to the Drosophila ether-a-go-go K+ channel. J Gen Physiol 109:301-311.
51. Tareilus E, Roux M, Qin N, Olcese R, Zhou J, Stefani E, Birnbaumer L (1997) A Xenopus oocyte beta subunit: evidence for a role in the assembly/expression of voltage-gated calcium channels that is separate from its role as a regulatory subunit. Proc Natl Acad Sci USA 94:1703-1708.
52. Turner TJ, Adams ME, Dunlap K (1992) Calcium channels coupled to glutamate release identified by omega-Aga-IVA. Science 258:310-313.
53. Wang YX, Bezprozvannaya S, Bowersox SS, Nadasdi L, Miljanich G, Mezo G, Silva D, Tarczy-Hornoch K, Luther RR (1998) Peripheral versus central potencies of N-type voltage-sensitive calcium channel blockers. Naunyn Schmiedebergs Arch Pharmacol 357:159-168.
54. Welling A, Ludwig A, Zimmer S, Klugbauer N, Flockerzi V, Hofmann F (1997) Alternatively spliced IS6 segments of the alpha 1C gene determine the tissue-specific dihydropyridine sensitivity of cardiac and vascular smooth muscle L-type Ca2+ channels. Circ Res 81:526-532.
55. Wheeler DB, Randall A, Tsien RW (1994) Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264:107-111.
56. Williams ME, Brust PF, Feldman DH, Patthi S, Simerson S, Maroufi A, McCue AF, Velicelebi G, Ellis SB, Harpold MM (1992) Structure and functional expression of an ω-Conotoxin-sensitive human N-type calcium channel. Science 257:389-395.
57. Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: Methods in neuronal modeling (Koch C, Segev I, eds), pp 97-134. Cambridge, MA: MIT.
58. Yamada Y, Masuda K, Li Q, Ihara Y, Kubota A, Miura T, Nakamura K, Fujii Y, Seino S, Seino Y (1995) The structures of the human calcium channel alpha 1 subunit (CACNL1A2) and beta subunit (CACNLB3) genes. Genomics 27:312-319.
59. 2+ channels in the kidney. Proc Natl Acad Sci USA 89:10494-10498.
60. Zamponi GW, Snutch TP (1998) Modulation of voltage-dependent calcium channels by G proteins. Curr Opin Neurobiol 8:351-356.
61. Zamponi GW, Soong TW, Bourinet E, Snutch TP (1996) Beta subunit coexpression and the alpha1 subunit domain I-II linker affect piperidine block of neuronal calcium channels. J Neurosci 16:2430-2443.
62. Zhang JF, Ellinor PT, Aldrich RW, Tsien RW (1994) Molecular determinants of voltage-dependent inactivation in calcium channels. Nature 372:97-100.
63. Zuhlke RD, Bouron A, Soldatov NM, Reuter H (1998) Ca2+ channel sensitivity toward the blocker isradipine is affected by alternative splicing of the human alpha1C subunit gene. FEBS Lett 427:220-224.