Constitutive activation of delayed-rectifier potassium channels by a Src family tyrosine kinase in Schwann cells

EMBO Journal

Volumn 17, Issue 16, 1998, Pages 4723-4734

  Sobko, Alexander ^a   Peretz, Asher ^a   Attali, Bernard ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

K+ channels; Myelination; Proliferation; Schwann cell; Src kinase

Indexed keywords

GENISTEIN; HERBIMYCIN A; POTASSIUM CHANNEL; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; MOUSE; MYELINATION; NERVE CELL PLASTICITY; NERVE GROWTH; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCHWANN CELL; SCIATIC NERVE;

ANIMALS; BENZOQUINONES; CELL DIVISION; CELLS, CULTURED; DELAYED RECTIFIER POTASSIUM CHANNELS; ENZYME INHIBITORS; GENISTEIN; ION CHANNEL GATING; LACTAMS, MACROCYCLIC; MICE; PHOSPHORYLATION; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; QUINONES; RECOMBINANT PROTEINS; SCHWANN CELLS; SCIATIC NERVE; SHAB POTASSIUM CHANNELS; SRC-FAMILY KINASES; TYROSINE;

ANIMALIA;

EID: 0032541410     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.16.4723     Document Type: Article

References (72)

1. Amedee,T., Ellie,E., Dupouy,B. and Vincent,J.D. (1991) Voltage-dependent calcium and potassium channels in Schwann cells cultured from dorsal root ganglia of the mouse. J. Physiol., 441, 35-56.
2. Atkinson,E.A., Ostergaard,H., Kane,K., Pinkosi,M., Caputo,A. and Olszowy,M.J. (1996) A physical interaction between the cell death protein Fas and the tyrosine kinase p59fynT. J. Biol. Chem., 271, 5968-5971.
3. Attali,B., Wang,N., Kolot,A., Sobko,A., Cherepanov,V. and Soliven,B. (1997) Characterization of delayed rectifier Kv channels in oligodendrocytes and progenitor cells. J. Neurosci., 17, 8234-8245.
4. Bare,D.J., Lauder,J.M., Wilkie,M.B. and Maness,P.F. (1993) p59fyn in rat brain is localized in developing axonal tracts and subpopulations of adult neurons and glia. Oncogene, 8, 1429-1436.
5. Barres,B.A., Chun,L.L.Y. and Corey,D.P. (1990) Ion channels in vertebrate glia. Annu. Rev. Neurosci., 13, 441-474.
6. Bekele-Arcuri,Z., Matos,M.F., Manganas,L., Strassle,B.W., Monaghan, M.M., Rhodes,K.J. and Trimmer,J.S. (1996) Generation and characterization of subunit-specific monoclonal antibodies to K+ channel α- and β-subunit polypeptides. Neuropharmacology, 35, 851-865.
7. Bolen,J.P. (1993) Nonreceptor tyrosine protein kinases. Oncogene, 8, 2025-2031.
8. Bowlby,M.R., Fadool,D.A., Holmes,T.C. and Levitan,I.B. (1997) Modulation of the Kv1.3 potassium channel by receptor tyrosine kinases. J. Gen. Physiol, 110, 601-610.
9. Boxall,A.R. and Lancaster,B. (1998) Tyrosine kinases and synaptic transmission. Eur. J. Nturosci., 10, 2-7.
10. Brockes,J.P., Fields,K.L. and Raff,M.C. (1979) Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res., 165, 105-118.
11. Cantley,L.C. and Songyang,Z. (1997) Specificity in protein-tyrosine kinase signaling. In Corbin,J. and Francis,S. (eds), Signal Transduction in Health and Disease. Advances in Second Messenger and Phosphoprotein Research. Lippincott-Raven Publishers, PA, pp. 41-48.
12. Chiu,S.Y. (1991) Functions and distribution of voltage-gated sodium and potassium channels in mammalian Schwann cells. Glia, 4, 541-558.
13. Chiu,S.Y. and Wilson,G.F. (1989) The role of potassium channels in Schwann cell proliferation in Wallerian degeneration of expiant rabbit sciatic nerve. J. Physiol., 408, 199-222.
14. Chiu,S.Y., Scherer,S.S., Blonski,M., Kang,S.S. and Messing,A. (1994) Axons regulate the expression of Shaker-like potassium channel genes in Schwann cells in perpheral nerve. Glia, 12, 1-11.
15. Courtneidge,S.A. and Fumagalli S. (1994) A mitotic function for Src? Trends Cell Biol., 4, 337-345.
16. Du,J., Zhang,L. Weiser,M., Rudy,B. and McBain,C.J. (1996) Developmental expression and functional characterization of the potassium-channel subunit kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci., 16, 506-518.
17. ErpeI,T. and Courtneidge,S.A. (1995) Src family protein tyrosine kinases and cellular signal tranduction pathways. Curr. Opin. Cell Biol., 7, 176-182.
18. 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.
19. + channel β subunit to specifically enhance Kv2.2 (CDRK) expression. J. Biol. Chem., 271, 26341-26348.
20. Frech,G.C., VanDongen,A.M., Schuster,G., Brown,A.M. and Joho,R.H. (1989) A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature, 340, 642-645.
21. Fuhrer,C., Sugiyama,J.E., Taylor,R.G. and Hall,Z.W. (1997) Association of muscle-specific kinase MuSK with the acetylcholine receptor in mammalian muscle. EMBO J., 16, 4951-4960.
22. 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.
23. Grinspan,J.B., Marchionni,M.A., Reeves,M., Coulaloglou,M. and Scherer,S.S. (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neurcgulin receptors and the role of neuregulins. J. Neurosci., 16, 6107-6118.
24. Hamill,O.P., Marty,A., Neher,E., Sakinann,B. and Sigworth,F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflug. Arch., 391, 85-100.
25. Holmes,T.C., Fadool,D.A. and Levitan,I.B. (1996a) Tyrosine phosphorylation of the Kv1.3 potassium channel. J. Neumsci., 16, 1581-1590.
26. Holmes,T.C., Fadool,D.A., Ren,R. and Levitan,J.B. (1996b) Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science, 274, 2089-2091.
27. + currents in cultured Schwann cells is controlled by extracelllar pH. Eur. J. Physiol., 415, 22-28.
28. 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.
29. Hugnot,J.P., Salinas,M., Lesage,F., Guillemare,E., de Weille,J., Heurteaux,C., Mattei,M.G. and Lazdunski,M. (1996) Kv8.1, a new neuronal potassium channel subunit with specific inhibitory properties towards Shab and Shaw channels. EMBO J., 15, 3322-3331.
30. Jessen,K.R., Brennan,A., Morgan,L., Mirsky,R., Kent,A., Hashimoto,Y. and Gavrilovic,J. (1994) The Schwann cell precursor and its fate: a study of cell death and differentiation during gliogenesis in rat embryonic nerves. Neuron, 12, 509-527.
31. Jonas,E.A. and Kaczmarek,L.K. (1996) Regulation of potassium channels by protein kinases. Curr. Opin. Neurobiol., 6, 318-323.
32. Jonas,E.A., Knox,R.J., Kaczmarek,L.K. and Schwartz,J.H. (1996) Insulin receptor in Aplysia neurons: characterization, molecular cloning and modulation of ion currents. J. Neurosci., 16, 1645-1658.
33. Kohr,G, and Seeburg,P.H. (1996) Subtype-specific regulation of recombinam NMDA receptor-channels by protein tyrosine kinases of the Src family. J. Physiol., 492.2, 445-452.
34. Konishi,T. (1989) Voltage-dependent potassium channels in mouse Schwann cells. J.Physiol., 411, 115-130.
35. Laemmli,E.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
36. LeBeau,J.M., Tedeschi B and Walter,G. (1991) Increased expression of pp60c-Src protein-tyrosine kinase during peripheral nerve regeneration. Neurosci. Res., 28, 299-309.
37. 2+-induced regulation of ion channel and MAP kinase functions. Nature, 376, 737-745.
38. + channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J. Neurosci., 15, 3840-3851.
39. Mi,H., Deerink,T.J., Ellisman,M. and Schwarz,T.L. (1995) Differential distribution of closely related potassium channels in rat Schwann cells. J. Neurosci., 15, 3761-3774.
40. Migita,K., Eguchi,K., Kawabe,Y. and Nagataki,S. (1995) Tyrosine phosphorylation participates in peripheral T-cell activation and programmed cell death. Immunology, 85, 550-555.
41. Mirsky,R. and Jessen,K.R. (1996) Schwann cell development, differentiation and myelination. Curr. Opin. Neurobiol., 6, 89-96.
42. Moarefi,I., LaFevre-Bernt,M., Sicheri,F., Huse,M., Lee,C.-H., Kuriyan,J. and Miller,W.T. (1997) Activation of the Src family tyrosine kinase Hck by SH3 domain displacement. Nature, 385, 650-653.
43. Pappas,C.A. and Ritchie,J.M. (1998) Effect of specific ion channel blockers on cultured Schwann cell proliferation. Glia, 22, 113-120.
44. i. Neuroreport, 6, 193-196.
45. + channel in oxygen-sensitive pulmonary artery myocytes. EMBO J., 16, 6615-6625.
46. Prevarskaya,N.B., Skryma,R.N., Vacher,P., Daniel,N., Djiane,J. and Dufy,B. (1995) Role of tyrosine phosphorylation in potassium channel activation. J. Biol. Chem., 270, 24292-24299.
47. Qian,D., Lev,S., van Oers,N.S., Dikic,I., Schlessinger,J. and Weiss,A. (1997) Tyrosine phosphorylation of Pyk2 is selectively regulated by Fyn during TCR signaling. J. Exp. Med., 185, 1253-1259.
48. Ritchie,J.M. (1992) Voltage-gated ion channels in Schwann cells and glia. Trends Neurosci., 15, 345-351.
49. 2 for fibroblast cell division. Science, 269, 1567-1569.
50. Ross,C.A., Wright,G.E., Resh,M.D., Pearson,C.A. and Snyder,S.H. (1988) Brain-specific Src family oncogene mRNA mapped in rat brain by in situ hybridization. Proc. Natl Acad. Sci. USA, 85, 9831-9835.
51. Salinas,M., Duprat,F., Heurteaux,C., Hugnot,J.P. and Lazdunski,M. (1997a) New modulatory α subunits for mammalian Shab K+ channels. J. Biol. Chem., 272, 24371-24379.
52. + channel activity by the Kv8.1 subunit. J. Biol. Chem., 272, 8774-8780.
53. Songyang,Z. et al. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell, 72, 767-778.
54. Songyang,Z. et al. (1995) Catalytic specificity of protein-tyrosine kinases is critical for selective signalling. Nature, 373, 536-539.
55. Sontheimer,H. (1994) Voltage-dependent ion channels in glial cells. Glia, 11, 156-172.
56. Sontheimer,H. (1995) Glial neuronal interactions: a physiological perspective. Neuroscientist, 1, 328-337.
57. 0 expression and DNA synthesis by insulin-like growth factors in vitro. Eur. J. Neurosci., 8, 553-564.
58. Swope,S.L. and Huganir,R.L. (1994) Binding of nicotinic acetylcholine receptor to SH2 domains of Fyn and fyk protein tyrosine kinases. J. Biol. Chem., 269, 29817-29824.
59. Syroid.D., Maycox,P., Burrola,P., Liu,N.,Wen, D and Lemke G. (1996) Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc. Natl Acad. Sci. USA, 93, 9229-9234.
60. + channel in T lymphocytes upon Fas stimulation. J. Biol. Chem., 271, 20465-20469.
61. Thomas,S.M. and Brugge,J.S. (1997) Cellular functions regulated by Src family kinases. Ann. Rev. Cell. Dev. Biol., 13, 513-609.
62. Trachtenberg,J.T. and Thompson,W.J. (1996) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factoc Nature, 379, 174-177.
63. Trotter,J., Boulter,C.A., Sontheimer,H., Schachner,M. and Wagner,E.F. (1989) Expression of v-Src arrests murine glial cell differentiation. Oncogene, 4, 457-464.
64. Tsai,W., Morielli,A.D. and Peralta,E.G. (1997) The ml muscarinic acetylcholine receptor transactivates the EGF receptor to modulate ion channel activity. EMBO J., 16, 4597-4605.
65. Uehara,Y. and Fukazawa,H. (1991) Use and selectivity of Herbimycin A as inhibitor of protein-tyrosine kinases. In Hunter,T. and Sefton,B.M. (eds). Protein Phosphorylation. Academic Press, San Diego, CA, pp. 370-378.
66. Umemori,H., Wanaka,A., Kato,H., Takeuchi,M., Tohyama,M. and Yamamoto,T. (1992) Specific expressions of Fyn and Lyn, lymphocyte antigen receptor-associated tyrosine kinases, in the central nervous system. Mol. Brain Res., 16, 303-310.
67. Umemori,H., Sato,S., Yagi,T., Aizawa,S. and Yamamoto,T. (1994) Initial events of myelination involve Fyn tyrosine kinase signalling. Nature, 367, 572-576.
68. Wilson,G.F. and Chiu,S.Y. (1990) Potassium channel regulation in Schwann cells during early developmental myelinogenesis. J. Neurosci., 10, 1615-1625.
69. Wilson,G.F. and Chiu,S.Y. (1993) Mitogenic factors regulate ionic channels in Schwann cells cultured from newborn rat sciatic nerve. J. Physiol., 470, 501-520.
70. Yu,S.P. et al (1997) Mediation of neuronal apoptosis by enhancement of outward potassium current. Science, 278, 114-117.
71. Yu,X.-M., Askalan,R., Keil II,G.J. and Salter,M.W. (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science, 275, 674-678.
72. Zorick,T.S. and Lemke,G. (1996) Schwann cell differentiation. Curr. Opin. Cell. Biol., 8, 870-876.