Multifaceted modulation of K + channels by protein-tyrosine phosphatase ε tunes neuronal excitability

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27614-27628

  Ebner Bennatan, Sharon ^a   Patrich, Eti ^a   Peretz, Asher ^a   Kornilov, Polina ^a   Tiran, Zohar ^b   Elson, Ari ^b   Attali, Bernard ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AFTERHYPERPOLARIZATION; BRAIN CORTEX; CHANNEL ACTIVITY; CHANNEL PROTEINS; CHO CELL; CORTICAL NEURONS; CULTURED CORTICAL NEURONS; DEPHOSPHORYLATIONS; DISCHARGE FREQUENCY; ION CHANNEL; K+ CHANNELS; POTASSIUM CHANNELS; PROTEIN-TYROSINE KINASE; PROTEIN-TYROSINE PHOSPHATASE; SRC-KINASE; SYNAPTIC PLASTICITY; TYROSINE PHOSPHATASE; TYROSINE PHOSPHORYLATION; WILD TYPES;

AMINO ACIDS; DEPOLARIZATION; MAMMALS; PHOSPHATASES; PHOSPHORYLATION; PROTEINS;

NEURONS;

DELAYED RECTIFIER POTASSIUM CHANNEL; PROTEIN TYROSINE PHOSPHATASE EPSILON;

ADULT ANIMAL; AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; BRAIN CORTEX; CHO CELL; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC SHOCK; ELECTROPHYSIOLOGY; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; MOUSE; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NEWBORN; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SEIZURE; SPIKE; UPREGULATION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; CEREBRAL CORTEX; CHO CELLS; CRICETINAE; CRICETULUS; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; POTASSIUM CHANNELS, VOLTAGE-GATED; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 4;

EID: 84864994878     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342519     Document Type: Article

References (68)

1. Jonas, E. A., and Kaczmarek, L. K. (1996) Regulation of potassium channels by protein kinases. Curr. Opin. Neurobiol. 6, 318-323
2. Levitan, I. B. (1994) Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu. Rev. Physiol. 56, 193-212
3. Grant, S. G., O'Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P., and Kandel, E. R. (1992) Impaired long term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258, 1903-1910
4. Lu, Y. M., Roder, J. C., Davidow, J., and Salter, M. W. (1998) Src activation in the induction of long term potentiation in CA1 hippocampal neurons. Science 279, 1363-1367
5. Petrone, A., Battaglia, F., Wang, C., Dusa, A., Su, J., Zagzag, D., Bianchi, R., Casaccia-Bonnefil, P., Arancio, O., and Sap, J. (2003) Receptor protein-tyrosine phosphatase α is essential for hippocampal neuronal migration and long term potentiation. EMBO J. 22, 4121-4131
6. Uetani, N., Kato, K., Ogura, H., Mizuno, K., Kawano, K., Mikoshiba, K., Yakura, H., Asano, M., and Iwakura, Y. (2000) Impaired learning with enhanced hippocampal long term potentiation in PTPδ-deficient mice. EMBO J. 19, 2775-2785
7. Ahn, M., Beacham, D., Westenbroek, R. E., Scheuer, T., and Catterall, W. A. (2007) Regulation of Na(v)1.2 channels by brain-derived neurotrophic factor, TrkB, and associated Fyn kinase. J. Neurosci. 27, 11533-11542
8. Fadool, D. A., Holmes, T. C., Berman, K., Dagan, D., and Levitan, I. B. (1997) Tyrosine phosphorylation modulates current amplitude and kinetics of a neuronal voltage-gated potassium channel. J. Neurophysiol. 78, 1563-1573
9. Ratcliffe, C. F., Qu, Y., McCormick, K. A., Tibbs, V. C., Dixon, J. E., Scheuer, T., and Catterall, W. A. (2000) A sodium channel signaling complex. Modulation by associated receptor protein-tyrosine phosphatase β. Nat. Neurosci. 3, 437-444
10. Rudy, B., and McBain, C. J. (2001) Kv3 channels. Voltage-gated K+ channels designed for high frequency repetitive firing. Trends Neurosci. 24, 517-526
11. Wang, Y. T., and Salter, M. W. (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369, 233-235
12. Wang, Y. T., Yu, X. M., and Salter, M. W. (1996) Ca2+-independent reduction of N-methyl-D-aspartate channel activity by protein-tyrosine phosphatase. Proc. Natl. Acad. Sci. U.S.A. 93, 1721-1725
13. Tsai, W., Morielli, A. D., Cachero, T. G., and Peralta, E. G. (1999) Receptor protein-tyrosine phosphatase α participates in the m1 muscarinic acetylcholine receptor-dependent regulation of Kv1.2 channel activity. EMBO J. 18, 109-118
14. Imbrici, P., Tucker, S. J., D'Adamo, M. C., and Pessia, M. (2000) Role of receptor protein-tyrosine phosphatase α (RPTPα) and tyrosine phosphorylation in the serotonergic inhibition of voltage-dependent potassium channels. Pflugers Arch. 441, 257-262
15. Fadool, D. A., and Levitan, I. B. (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J. Neurosci. 18, 6126-6137
16. Holmes, T. C., Fadool, D. A., Ren, R., and Levitan, I. B. (1996) Association of Src-tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 274, 2089-2091
17. Szabò, I., Gulbins, E., Apfel, H., Zhang, X., Barth, P., Busch, A. E., Schlottmann, K., Pongs, O., and Lang, F. (1996) Tyrosine phosphorylation-dependent suppression of a voltage-gated K+ channel in T lymphocytes upon Fas stimulation. J. Biol. Chem. 271, 20465-20469
18. Nitabach, M. N., Llamas, D. A., Thompson, I. J., Collins, K. A., and Holmes, T. C. (2002) Phosphorylation-dependent and phosphorylation-independent modes of modulation of shaker family voltage-gated potassium channels by SRC family protein-tyrosine kinases. J. Neurosci. 22, 7913-7922
19. Gamper, N., Stockand, J. D., and Shapiro, M. S. (2003) Subunit-specific modulation of KCNQ potassium channels by Src-tyrosine kinase. J. Neurosci. 23, 84-95
20. Jia, Q., Jia, Z., Zhao, Z., Liu, B., Liang, H., and Zhang, H. (2007) Activation of epidermal growth factor receptor inhibits KCNQ2/3 current through two distinct pathways. Membrane PtdIns(4,5)P2 hydrolysis and channel phosphorylation. J. Neurosci. 27, 2503-2512
21. Li, Y., Langlais, P., Gamper, N., Liu, F., and Shapiro, M. S. (2004) Dual phosphorylations underlie modulation of unitary KCNQ K+ channels by Src-tyrosine kinase. J. Biol. Chem. 279, 45399-45407
22. Peretz, A., Sobko, A., and Attali, B. (1999) Tyrosine kinases modulate K+ channel gating in mouse Schwann cells. J. Physiol. 519, 373-384
23. Sobko, A., Peretz, A., and Attali, B. (1998) Constitutive activation of delayed-rectifier potassium channels by a src family tyrosine kinase in Schwann cells. EMBO J. 17, 4723-4734
24. Peretz, A., Gil-Henn, H., Sobko, A., Shinder, V., Attali, B., and Elson, A. (2000) Hypomyelination and increased activity of voltage-gated K+ channels in mice lacking protein-tyrosine phosphatase ε. EMBO J. 19, 4036-4045
25. Tiran, Z., Peretz, A., Sines, T., Shinder, V., Sap, J., Attali, B., and Elson, A. (2006) Tyrosine phosphatases ε and α perform specific and overlapping functions in regulation of voltage-gated potassium channels in Schwann cells. Mol. Biol. Cell 17, 4330-4342
26. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100
27. Tiran, Z., Peretz, A., Attali, B., and Elson, A. (2003) Phosphorylation-dependent regulation of Kv2.1 channel activity at tyrosine 124 by Src and by protein-tyrosine phosphatase α. J. Biol. Chem. 278, 17509-17514
28. Fakler, B., and Adelman, J. P. (2008) Control of K(Ca) channels by calcium nano/microdomains. Neuron 59, 873-881
29. Latorre, R., and Brauchi, S. (2006) Large conductance Ca2+-activated K+ (BK) channel. Activation by Ca2+ and voltage. Biol. Res. 39, 385-401
30. Adams, P. R., Constanti, A., Brown, D. A., and Clark, R. B. (1982) Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones. Nature 296, 746-749
31. Storm, J. F. (1987) Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol. 385, 733-759
32. Womack, M. D., and Khodakhah, K. (2002) Characterization of large conductance Ca2+-activated K+ channels in cerebellar Purkinje neurons. Eur. J. Neurosci. 16, 1214-1222
33. Chung, S. K., Reinhart, P. H., Martin, B. L., Brautigan, D., and Levitan, I. B. (1991) Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel. Science 253, 560-562
34. Reinhart, P. H., Chung, S., Martin, B. L., Brautigan, D. L., and Levitan, I. B. (1991) Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J. Neurosci. 11, 1627-1635
35. Alioua, A., Mahajan, A., Nishimaru, K., Zarei, M. M., Stefani, E., and Toro, L. (2002) Coupling of c-Src to large conductance voltage- and Ca2+-activated K+ channels as a new mechanism of agonist-induced vasoconstriction. Proc. Natl. Acad. Sci. U.S.A. 99, 14560-14565
36. Ling, S., Sheng, J. Z., and Braun, A. P. (2004) The calcium-dependent activity of large conductance, calcium-activated K+ channels is enhanced by Pyk2- and Hck-induced tyrosine phosphorylation. Am. J. Physiol. Cell Physiol. 287, C698-C706
37. Ling, S., Woronuk, G., Sy, L., Lev, S., and Braun, A. P. (2000) Enhanced activity of a large conductance, calcium-sensitive K+ channel in the presence of Src-tyrosine kinase. J. Biol. Chem. 275, 30683-30689
38. Tian, L., McClafferty, H., Chen, L., and Shipston, M. J. (2008) Reversible tyrosine protein phosphorylation regulates large conductance voltage- and calcium-activated potassium channels via cortactin. J. Biol. Chem. 283, 3067-3076
39. Zhou, R., Liu, L., and Hu, D. (2005) Involvement of BKCa α subunit tyrosine phosphorylation in vascular hyporesponsiveness of superior mesenteric artery following hemorrhagic shock in rats. Cardiovasc. Res. 68, 327-335
40. Huang, X. Y., Morielli, A. D., and Peralta, E. G. (1993) Tyrosine kinase-dependent suppression of a potassium channel by the G protein-coupled m1 muscarinic acetylcholine receptor. Cell 75, 1145-1156
41. Du, J., Haak, L. L., Phillips-Tansey, E., Russell, J. T., and McBain, C. J. (2000) Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K+ channel subunit Kv2.1. J. Physiol. 522, 19-31
42. Misonou, H., Mohapatra, D. P., and Trimmer, J. S. (2005) Kv2.1, a voltage-gated K+ channel critical to dynamic control of neuronal excitability. Neurotoxicology 26, 743-752
43. Murakoshi, H., and Trimmer, J. S. (1999) Identification of the Kv2.1 K+ channel as a major component of the delayed rectifier K+ current in rat hippocampal neurons. J. Neurosci. 19, 1728-1735
44. Gil-Henn, H., and Elson, A. (2003) Tyrosine phosphatase-ε activates Src and supports the transformed phenotype of Neu-induced mammary tumor cells. J. Biol. Chem. 278, 15579-15586
45. Granot-Attas, S., Luxenburg, C., Finkelshtein, E., and Elson, A. (2009) Protein-tyrosine phosphatase ε regulates integrin-mediated podosome stability in osteoclasts by activating Src. Mol. Biol. Cell 20, 4324-4334
46. Azouz, R., Jensen, M. S., and Yaari, Y. (1996) Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. 492, 211-223
47. Magee, J. C., and Carruth, M. (1999) Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 82, 1895-1901
48. Metz, A. E., Jarsky, T., Martina, M., and Spruston, N. (2005) R-type calcium channels contribute to after depolarization and bursting in hippocampal CA1 pyramidal neurons. J. Neurosci. 25, 5763-5773
49. Golomb, D., Yue, C., and Yaari, Y. (2006) Contribution of persistent Na+ current and M-type K+ current to somatic bursting in CA1 pyramidal cells. Combined experimental and modeling study. J. Neurophysiol. 96, 1912-1926
50. Su, H., Alroy, G., Kirson, E. D., and Yaari, Y. (2001) Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J. Neurosci. 21, 4173-4182
51. Yue, C., Remy, S., Su, H., Beck, H., and Yaari, Y. (2005) Proximal persistent Na+ channels drive spike after depolarizations and associated bursting in adult CA1 pyramidal cells. J. Neurosci. 25, 9704-9720
52. Chen, S., Yue, C., and Yaari, Y. (2005) A transitional period of Ca2+-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells. J. Physiol. 567, 79-93
53. Christie, B. R., Eliot, L. S., Ito, K., Miyakawa, H., and Johnston, D. (1995) Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J. Neurophysiol. 73, 2553-2557
54. Hu, H., Vervaeke, K., and Storm, J. F. (2007) M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J. Neurosci. 27, 1853-1867
55. Peretz, A., Sheinin, A., Yue, C., Degani-Katzav, N., Gibor, G., Nachman, R., Gopin, A., Tam, E., Shabat, D., Yaari, Y., and Attali, B. (2007) Pre- and postsynaptic activation of M-channels by a novel opener dampens neuronal firing and transmitter release. J. Neurophysiol. 97, 283-295
56. Shah, M. M., Migliore, M., Valencia, I., Cooper, E. C., and Brown, D. A. (2008) Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 7869-7874
57. Yue, C., and Yaari, Y. (2004) KCNQ/M channels control spike after depolarization and burst generation in hippocampal neurons. J. Neurosci. 24, 4614-4624
58. Yue, C., and Yaari, Y. (2006) Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J. Neurophysiol. 95, 3480-3495
59. Metz, A. E., Spruston, N., and Martina, M. (2007) Dendritic D-type potassium currents inhibit the spike after depolarization in rat hippocampal CA1 pyramidal neurons. J. Physiol. 581, 175-187
60. Faber, E. S., and Sah, P. (2003) Calcium-activated potassium channels. Multiple contributions to neuronal function. Neuroscientist 9, 181-194
61. Smart, S. L., Lopantsev, V., Zhang, C. L., Robbins, C. A., Wang, H., Chiu, S. Y., Schwartzkroin, P. A., Messing, A., and Tempel, B. L. (1998) Deletion of the K(V)1.1 potassium channel causes epilepsy in mice. Neuron 20, 809-819
62. Brew, H. M., Gittelman, J. X., Silverstein, R. S., Hanks, T. D., Demas, V. P., Robinson, L. C., Robbins, C. A., McKee-Johnson, J., Chiu, S. Y., Messing, A., and Tempel, B. L. (2007) Seizures and reduced life span in mice lacking the potassium channel subunit Kv1.2 but hypoexcitability and enlarged Kv1 currents in auditory neurons. J. Neurophysiol. 98, 1501-1525
63. Gu, N., Vervaeke, K., and Storm, J. F. (2007) BK potassium channels facilitate high frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J. Physiol. 580, 859-882
64. Matthews, E. A., Weible, A. P., Shah, S., and Disterhoft, J. F. (2008) The BK-mediated fAHP is modulated by learning a hippocampus-dependent task. Proc. Natl. Acad. Sci. U.S.A. 105, 15154-15159
65. Jaffe, D. B., Wang, B., and Brenner, R. (2011) Shaping of action potentials by type I and type II large-conductance Ca2+-activated K+ channels. Neuroscience 192, 205-218
66. Jin, W., Sugaya, A., Tsuda, T., Ohguchi, H., and Sugaya, E. (2000) Relationship between large conductance calcium-activated potassium channel and bursting activity. Brain Res. 860, 21-28
67. Du, W., Bautista, J. F., Yang, H., Diez-Sampedro, A., You, S. A., Wang, L., Kotagal, P., Lüders, H. O., Shi, J., Cui, J., Richerson, G. B., and Wang, Q. K. (2005) Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat. Genet. 37, 733-738
68. Brenner, R., Chen, Q. H., Vilaythong, A., Toney, G. M., Noebels, J. L., and Aldrich, R. W. (2005) BK channel β4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat. Neurosci. 8, 1752-1759