Interaction of syntaxin with a single Kv1.1 channel: A possible mechanism for modulating neuronal excitability

Pflugers Archiv European Journal of Physiology

Volumn 454, Issue 3, 2007, Pages 477-494

  Michaelevski, Izhak ^a   Korngreen, Alon ^b   Lotan, Ilana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b BAR ILAN UNIVERSITY   (Israel)

Author keywords

Kv1.1; Shunting inhibition; Single channel; Subconductance levels; Syntaxin 1A

Indexed keywords

POTASSIUM CHANNEL KV1.1; SYNTAXIN 1A;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL STIMULATION; CHANNEL GATING; CONDUCTANCE; CONTROLLED STUDY; DEPOLARIZATION; KINETICS; MATHEMATICAL MODEL; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER; NEUROPHYSIOLOGY; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEADY STATE; SYNAPSE;

ANIMALS; FEMALE; KINETICS; KV1.1 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; OOCYTES; PATCH-CLAMP TECHNIQUES; RECOMBINANT PROTEINS; SYNTAXIN 1; XENOPUS; XENOPUS PROTEINS;

EID: 34248353786     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0223-5     Document Type: Article

References (46)

1. Veh RW, Lichtinghagen R, Sewing S, Wunder F, Grumbach IM, Pongs O (1995) Immunohistochemical localization of five members of the Kv1 channel subunits: contrasting subcellular locations and neuron-specific co-localizations in rat brain. Eur J Neurosci 7:2189-2205
2. Wang H, Allen ML, Grigg JJ, Noebels JL, Tempel BL (1995) Hypomyelination alters K+ channel expression in mouse mutants shiverer and Trembler. Neuron 15:1337-1347
3. Rasband MN, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, Shrager P (1998) Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18: 36-47
4. Wang H, Kunkel DD, Martin TM, Schwartzkroin PA, Tempel BL (1993) Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 365:75-79
5. Wang H, Kunkel DD, Schwartzkroin PA, Tempel BL (1994) Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J Neurosci 14:4588-4599
6. Grissmer S, Nguyen AN, Aiyar J, Hanson DC, Mather RJ, Gutman GA, Karmilowicz MJ, Auperin DD, Chandy KG (1994) Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45:1227-1234
7. Stuhmer W, Ruppersberg JP, Schroter KH, Sakmann B, Stocker M, Giese KP, Perschke A, Baumann A, Pongs O (1989) Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J 8:3235-3244
8. Meiri N, Ghelardini C, Tesco G, Galeotti N, Dahl D, Tomsic D, Cavallaro S, Quattrone A, Capaccioli S, Bartolini A, Alkon DL (1997) Reversible antisense inhibition of Shaker-like Kv1.1 potassium channel expression impairs associative memory in mouse and rat. Proc Natl Acad Sci USA 94:4430-4434
9. Shillito P, Molenaar PC, Vincent A, Leys K, Zheng W, van den Berg RJ, Plomp JJ, van Kempen GT, Chauplannaz G, Wintzen AR et al (1995) Acquired neuromyotonia: evidence for autoantibodies directed against K+ channels of peripheral nerves. Ann Neurol 38:714-722
10. Fili O, Michaelevski I, Bledi Y, Chikvashvili D, Singer-Lahat D, Boshwitz H, Linial M, Lotan I (2001) Direct interaction of a brain voltage-gated K+ channel with syntaxin 1A: functional impact on channel gating. J Neurosci 21:1964-1974
11. Bajjalieh SM, Scheller RH (1995) The biochemistry of neurotransmitter secretion. J Biol Chem 270:1971-1974
12. Sudhof TC (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653
13. Linial M, Parnas D (1996) Deciphering neuronal secretion: tools of the trade. Biochim Biophys Acta 1286:117-152
14. Bennett MK (1995) SNAREs and the specificity of transport vesicle targeting. Curr Opin Cell Biol 7:581-586
15. Lopantsev V, Tempel BL, Schwartzkroin PA (2003) Hyperexcitability of CA3 pyramidal cells in mice lacking the potassium channel subunit Kv1.1. Epilepsia 44:1506-1512
16. Sheng ZH, Rettig J, Cook T, Catterall WA (1996) Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379:451-454
17. Michaelevski I, Chikvashvili D, Tsuk S, Fili O, Lohse MJ, Singer-Lahat D, Lotan I (2002) Modulation of a brain voltage-gated K+ channel by syntaxin 1A requires the physical interaction of Gbetagamma with the channel. J Biol Chem 277:34909-34917
18. Jarvis SE, Magga JM, Beedle AM, Braun JE, Zamponi GW (2000) G protein modulation of N-type calcium channels is facilitated by physical interactions between syntaxin 1A and Gbetagamma. J Biol Chem 275:6388-6394
19. Jarvis SE, Zamponi GW (2001) Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J Neurosci 21:2939-2948
20. Bezprozvanny I, Zhong P, Scheller RH, Tsien RW (2000) Molecular determinants of the functional interaction between syntaxin and N-type Ca2+ channel gating. Proc Natl Acad Sci USA 97:13943-13948
21. Stanley EF, Mirotznik RR (1997) Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature 385:340-343
22. Dascal N, Lotan I, Karni E, Gigi A (1992) Calcium channel currents in Xenopus oocytes injected with rat skeletal muscle RNA. J Physiol 450:469-490
23. Singer-Lahat D, Dascal N, Lotan I (1999) Modal behavior of the Kv1.1 channel conferred by the Kvbeta1.1 subunit and its regulation by dephosphorylation of Kv1.1. Pflugers Arch 439:18-26
24. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209
25. Islas LD, Sigworth FJ (1999) Voltage sensitivity and gating charge in Shaker and Shab family potassium channels. J Gen Physiol 114:723-742
26. Qin F, Auerbach A, Sachs F (1997) Maximum likelihood estimation of aggregated Markov processes. Proc Biol Sci 264:375-383
27. Qin F, Auerbach A, Sachs F (2000) Hidden Markov modeling for single channel kinetics with filtering and correlated noise. Biophys J 79:1928-1944
28. Hodgkin AL, Huxley AF (1952) Propagation of electrical signals along giant nerve fibers. Proc R Soc Lond B Biol Sci 140:177-183
29. Hodgkin AL, Huxley AF (1952) Movement of sodium and potassium ions during nervous activity. Cold Spring Harb Symp Quant Biol 17:43-52
30. Hodgkin AL, Huxley AF, Katz B (1952) Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol 116:424-448
31. Keren N, Peled N, Korngreen A (2005) Constraining compartmental models using multiple voltage recordings and genetic algorithms. J Neurophysiol 94:3730-3742
32. Zheng J, Sigworth FJ (1997) Selectivity changes during activation of mutant Shaker potassium channels. J Gen Physiol 110:101-117
33. Zheng J, Sigworth FJ (1998) Intermediate conductances during deactivation of heteromultimeric Shaker potassium channels. J Gen Physiol 112:457-474
34. Condliffe SB, Zhang H, Frizzell RA (2004) Syntaxin 1A regulates ENaC channel activity. J Biol Chem 279:10085-10092
35. Chapman ML, Vandongen AM (2005) K channel subconductance levels result from heteromeric pore conformations. J Gen Physiol 126:87-103
36. Bezanilla F (2005) The origin of subconductance levels in voltage-gated K+ channels. J Gen Physiol 126:83-86
37. Cushman SJ, Nanao MH, Jahng AW, DeRubeis D, Choe S, Pfaffinger PJ (2000) Voltage dependent activation of potassium channels is coupled to T1 domain structure. Nat Struct Biol 7:403-407
38. Yao X, Liu W, Tian S, Rafi H, Segal AS, Desir GV (2000) Close association of the N terminus of Kv1.3 with the pore region. J Biol Chem 275:10859-10863
39. Wang G, Covarrubias M (2006) Voltage-dependent gating rearrangements in the intracellular T1-T1 interface of a K+ channel. J Gen Physiol 127:391-400
40. Yi BA, Minor DL Jr, Lin YF, Jan YN, Jan LY (2001) Controlling potassium channel activities: Interplay between the membrane and intracellular factors. Proc Natl Acad Sci USA 98:11016-11023
41. Chiu SY, Zhou L, Zhang CL, Messing A (1999) Analysis of potassium channel functions in mammalian axons by gene knockouts. J Neurocytol 28:349-364
42. Tan YP, Llano I (1999) Modulation by K+ channels of action potential-evoked intracellular Ca2+ concentration rises in rat cerebellar basket cell axons. J Physiol 520 Pt 1:65-78
43. Dodson PD, Barker MC, Forsythe ID (2002) Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J Neurosci 22:6953-6961
44. Rettig J, Heinemann SH, Wunder F, Lorra C, Parcej DN, Dolly JO, Pong O (1994) Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature 369:289-294
45. Rhodes KJ, Keilbaugh SA, Barrezueta NX, Lopez KL, Trimmer JS (1995) Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain. J Neurosci 15:5360-5371
46. Geiger JR, Jonas P (2000) Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 28:927-939