Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation

European Journal of Neuroscience

Volumn 12, Issue 6, 2000, Pages 1949-1960

  Cayabyab, Francisco S ^a   Khanna, Rajesh ^a   Jones, Owen T ^a   Schlichter, Lyanne C ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Kv channel regulation; Microglia activation; Oxidative stress; PSD 95; Tyrosine phosphorylation

Indexed keywords

GLUCOSE; LAVENDUSTIN A; OXYGEN; POTASSIUM; POTASSIUM CHANNEL; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CHANNEL GATING; CONTROLLED STUDY; DOWN REGULATION; MICROGLIA; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELLS, CULTURED; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KV1.3 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MICROGLIA; NERVE TISSUE PROTEINS; ONCOGENE PROTEIN PP60(V-SRC); OXIDATIVE STRESS; OXYGEN; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, WISTAR; SCORPION VENOMS; SRC-FAMILY KINASES; TRANSFECTION; TYROSINE;

EID: 0034118777     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00083.x     Document Type: Article

References (61)

1. Boulet, I., Ralph, S., Stanley, E., Lock, P., Dunn, A.R., Green, S.P. & Phillips, W.A. (1992) Lipopolysaccharide-and interferon-gamma-induced expression of hck and lyn tyrosine kinases in murine bone marrow-derived macrophages. Oncogene, 7, 703-710.
2. Bowlby, M.R., Fadool, D.A., Holmes, T.C. & Levitan, I.B. (1997) Modulation of the Kvl.3 potassium channel by receptor tyrosine kinases. J. Gen. Physiol., 110, 601-610.
3. Cai, Y.C. & Douglass, J. (1993) In vivo and in vitro phosphorylation of the T lymphocyte type n (Kvl.3) potassium channel. J. Biol. Chem., 268, 23720-23727.
4. Chung, I. & Schlichter, L.C. (1997) Regulation of native Kvl.3 channels by cAMP-dependent protein phosphorylation. J. Membr. Biol., 156, 73-85.
5. Ciesielski-Treska, J., Ulrich, G., Chasserot-Golaz, S. & Aunis, D. (1995) Immunocytochemical localisation of protein kinases Yes and Src in amoeboid microglia in culture: association of Yes kinase with vimentin intermediate filaments. Eur. J. Cell Biol., 68, 369-376.
6. 2+ channels. Am. J. Physiol., 266, C1650-C1655.
7. Combs, C.K., Johnson, D.E., Cannady, S.B., Lehman, T.M. & Landreth, G.E. (1999) Identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of beta-amyloid and prion proteins. J. Neurosci., 19, 928-939.
8. + channel in rat PC12 cells by hypoxia. J. Physiol. (Lond.), 502, 293-305.
9. - forming NADPH oxidase in microglia, monocytes, and neutrophils. J. Biol. Chem., 274, 15493-15499.
10. + channels to reactive oxygen species. Proc. Natl Acad. Sci. USA, 92, 11796-11800.
11. Eder, C. (1998) Ion channels in microglia (brain macrophages). Am. J. Physiol., 275, C327-C342.
12. Fadool, D.A., Holmes, T.C., Berman, K., Dagan, D. & Levitan, I.B. (1997) Tyrosine phosphorylation modulates current amplitude and kinetics of a neuronal voltage-gated potassium channel. J. Neurophysiol., 78, 1563-1573.
13. Fadool, D.A. & Levitan, I.B. (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J. Neurosci., 18, 6126-6137.
14. Fedoroff, S., Berezovskaya, O. & Maysinger, D. (1997) Role of colony stimulating factor-1 in brain damage caused by ischemia. Neurosci. Biobehav. Rev., 21, 187-191.
15. 2 release in adherent human neutrophils. J. Immun., 160, 5154-5162.
16. + channel profile of microglia at immunologically defined functional states. Neuroscience, 64, 183-191.
17. Garcia, M.L., Hanner, M., Knaus, H.-G., Koch, R., Schmalhofer, W., Slaughter, R.S. & Kaczorowski, G.J. (1997) Pharmacology of potassium channels. Adv. Pharmacol., 39, 425-471.
18. Gebicke-Haerter, P.J., Van Calker, D., Norenberg, W. & Illes, P. (1996) Molecular mechanisms of microglial activation, A. Implications for regeneration and neurodegenerative diseases. Neurochem. Int., 29, 1-12.
19. Gehrmann, J., Matsumoto, Y. & Kreutzberg, G.W. (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res. Rev., 20, 269-287.
20. Giulian, D. & Ingeman, J.E. (1988) Colony-stimulating factors as promoters of ameboid microglia. J. Neurosci., 8, 4707-4717.
21. Gulbins, E., Szabo, I., Baltzer, K. & Lang, F. (1997) Ceramide-induced inhibition of T lymphocyte voltage-gated channel is mediated by tyrosine kinases. Proc. Natl Acad. Sci. USA, 94, 7661-7666.
22. lck tyrosine kinase and Shaker type Kv1.3 potassium channel in T lymphocytes. J. Biol. Chem., 272, 26899-26904.
23. Holmes, T.C., Fadool, D.A. & Levitan, I.B. (1996a) Tyrosine phosphorylation of the Kv1.3 potassium channel. J. Neurosci., 16, 1581-1590.
24. Holmes, T.C., Fadool, D.A., Ren, R. & Levitan, I.B. (1996b) Association of src tyrosine kinases with a human potassium channel mediated by SH3 domain. Science, 274, 2089-2091.
25. Huang, X.Y., Morielli, A.D. & Peralta, E.G. (1993) Tyrosine kinase-dependent suppression of a potassium channel by the G protein-coupled ml muscarinic acetylcholine receptor. Cell, 75, 1145-1156.
26. Ilschner, S., Nolte, C. & Kettenmann, H. (1996) Complement factor C5a and epidermal growth factor trigger the activation of outward potassium currents in cultured murine microglia. Neuroscience, 73, 1109-1120.
27. Kettenmann, H., Hoppe, D., Gottmann, K., Banati, R. & Kreutzberg, G.W. (1990) Cultured microglial cells have a distinct pattern of membrane channels different from peritoneal macrophages. J. Neurosci. Res., 26, 278-287.
28. Khanna, R., Cayabyab, F.S., Jones, O.T. & Schlichter, L.C. (1998) Inhibition of Shaker-type Kv1.3 channels by src-family tyrosine kinases and anoxia in rat brain microglia. Soc. Neurosci. Abstr. 24, 1995.
29. Khanna, R., Chang, M.C., Joiner, W.J., Kaczmarek, L.K. & Schlichter, L.C. (1999a) hSK4/hIK1, a calmodulin-binding KCa channel in human T lymphocytes: roles in proliferation and volume regulation. J. Biol. Chem., 274, 14838-14849.
30. + channels orchestrate key functions of neuroimmune cells. Am. Physiol. Soc. Mtg. 'Biology of potassium channels: from molecules to disease'. Physiologist, 42, A21.
31. Kiefer, F., Brumel, J., Al-alawi, N., Latour, S., Cheng, A., Veillette, A., Grinstein, S. & Pawson, T. (1998) The syk protein tyrosine kinase is essential for Fcgamma receptor signaling in macrophages and neutrophils. Mol. Cell. Biol., 18, 4209-4220.
32. + channels by interaction with a family of membrane-associated guanylate kinases. Nature, 378, 85-88.
33. Kornau, H.C., Seeburg, P.H. & Kennedy, M.B. (1997) Interaction of ion channels and receptors with PDZ domain proteins. Curr. Opin. Neurobiol., 7, 368-373.
34. Korotzer, A.R. & Cotman, C.W. (1992) Voltage-gated currents expressed by rat microglia in culture. Glia, 6, 81-88.
35. Kotecha, S.A. & Schlichter, L.C. (1999) A Kv1.5-to-Kv1.3 switch in endogenous hippocampal microglia and a role in proliferation. J. Neurosci., 19, 10680-10693.
36. Kourie, J.L. (1998) Interaction of reactive oxygen species with ion transport mechanisms. Am. J. Physiol., 275, C1-C24.
37. Lewis, R.S. & Cahalan, M.D. (1995) Potassium and calcium channels in lymphocytes. Annu. Rev. Immunol., 13, 623-653.
38. c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol., 133, 895-910.
39. McDonald, D.R., Brunden, K.R. & Landreth, G.E. (1997) Amyloid fibrils activate tyrosine-dependent signaling and superoxide production in microglia. J. Neurosci., 17, 2284-2294.
40. Norenberg, W., Gebicke-Haerter, P.J. & Illes, P. (1994) Voltage-dependent potassium channels in activated rat microglia. J. Physiol. (Lond.), 475, 15-32.
41. Pawson, T. (1995) Protein modules and signalling networks. Nature, 373, 573-580.
42. Roy, L. & Schlichter, L.C. (1998) Ischemic activation of microglia in vitro: fluorescent and morphological analysis. Int. J. Dev. Neurosci., 16, 569.
43. + channels involved in mediating protein-protein interactions. Biochem. Biophys. Res. Commun., 232, 585-589.
44. + and Cl channels and their involvement in proliferation of rat microglial cells. Glia, 17, 225-236.
45. Schmidtmayer, J., Jacobsen, C., Miksch, G. & Sievers, J. (1994) Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: membrane currents. Glia, 12, 259-267.
46. Schrenzel, J., Serrander, L., Banfi, B., Nusse, O., Fouyouzi, R., Lew, D.P., Demaurex, N. & Krause, K.-H. (1998) Electron currents generated by the human phagocyte NADPH oxidase. Nature, 392, 734-737.
47. + channel Kv1 subtypes in synaptic membranes from bovine brain. Biochemistry, 36, 8195-8201.
48. Sobko, A., Peretz, A. & Attali, B. (1998a) Constitutive activation of delayed-rectifier potassium channels by a Src family tyrosine kinase in Schwann cells. EMBO J., 17, 4723-4734.
49. + channels in Schwann cells: developmental expression and role in proliferation. J. Neurosci., 18, 10398-10408.
50. Songyang, Z., Shoelson, S.E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W.G., King, F., Roberts, T., Ratnofsky, S. & Lechleider, R.J. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell, 72, 767-778.
51. Spranger, M., Kiprianova, I., Krempien, S. & Schwab, S. (1998) Reoxygenation increases the release of reactive oxygen intermediates in murine microglia. J. Cereb. Blood Flow Metab., 18, 670-674.
52. Streit, W.J., Walter, S.A. & Pennell, N.A. (1999) Reactive microgliosis. Prog. Neurobiol., 57, 563-581.
53. + channel in T lymphocyles upon Fas stimulation. J. Biol. Chem., 271, 20465-20469.
54. Szabo, I., Nilius, B., Zhang, X., Busch, A.E., Gulbins, E., Suessbrich, H. & Lang, F. (1997) Inhibitory effects of oxidants on n-type K+ channels in T lymphocytes and Xenopus oocytes. Pflugers Arch., 433, 626-632.
55. Tezuka, T., Umemori, H., Akiyama, T., Nakanishi, S. & Yamamoto, T. (1999) PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit NR2A. Proc. Natl Acad. Sci. USA, 96, 435-440.
56. Visentin, S., Agresti, C., Patrizio, M. & Levi, G. (1995) Ion channels in rat microglia and their different sensitivity to lipopolysaccharide and interferon-gamma. J. Neurosci. Res., 42, 439-451.
57. Vogt, M., Bauer, M.K., Ferrari, D. & Schulze-Osthoff, K. (1998) Oxidative stress and hypoxia/reoxygenation trigger CD95 (APO-1/Fas) ligand expression in microglial cells. FEBS Lett., 429, 67-72.
58. Wang, Y.-T. & Salter, M.W. (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature, 369, 233-235.
59. lyn tyrosine kinases. J. Biol. Chem., 271, 23464-23471.
60. Yu, X.M., Askalan, R., Keil, G.J. & Salter, M.W. (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science, 275, 674-678.
61. + channels in microglia. J. Gen. Physiol., III, 781-794.