Microglia Kv1.3 channels contribute to their ability to kill neurons

Journal of Neuroscience

Volumn 25, Issue 31, 2005, Pages 7139-7149

  Fordyce, Christopher B ^a,b   Jagasia, Ravi ^a,b   Zhu, Xiaoping ^a   Schlichter, Lyanne C ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

Anti inflammatory treatments; Kv channel roles; Kv expression; Microglia activation; Neuroinflammation; Neurotoxicity

Indexed keywords

4 AMINOPYRIDINE; AGITOXIN 2; ALPHA DENDROTOXIN; CHARYBDOTOXIN; DENDROTOXIN; LIPOPOLYSACCHARIDE; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROTOXIN; NITRIC OXIDE; PEROXYNITRITE; PHORBOL ESTER; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KCNQ1; POTASSIUM CHANNEL KV1.2; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.5; SUPEROXIDE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL KILLING; ENCEPHALITIS; HIPPOCAMPUS; MICROGLIA; NERVE CELL; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY BURST;

ANIMALS; ANIMALS, NEWBORN; CELL DEATH; CELLS, CULTURED; ELECTRIC CONDUCTIVITY; ENZYME ACTIVATION; KV1.3 POTASSIUM CHANNEL; MICROGLIA; NEURONS; NEUROTOXINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXYNITROUS ACID; RATS; RATS, WISTAR; RESPIRATORY BURST; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 23444436221     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1251-05.2005     Document Type: Article

References (61)

1. Ajmone-Cat MA, De Simone R, Nicolini A, Minghetti L (2003) Effects of phosphatidylserine on p38 mitogen activated protein kinase, cyclic AMP responding element binding protein and nuclear factor-kappaB activation in resting and activated microglial cells. J Neurochem 84:413-416.
2. Aloisi F (2001) Immune function of microglia. Glia 36:165-179.
3. Bal-Price A, Brown GC (2001) Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J Neurosci 21:6480-6491.
4. Bal-Price A, Matthias A, Brown GC (2002) Stimulation of the NADPH oxidase in activated rat microglia removes nitric oxide but induces peroxynitrite production. J Neurochem 80:73-80.
5. Banati RB, Rothe G, Valet G, Kreutzberg GW (1991) Respiratory burst activity in brain macrophages: a flow cytometric study on cultured rat microglia. Neuropathol Appl Neurobiol 17:223-230.
6. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, Legos JJ, Ehrhardt JA, Ohlstein EH, Hunter AJ, Harrison DC, Philpott K, Smith BR, Adams JL, Parsons AA (2001) Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med Res Rev 21:129-145.
7. Boje KM, Arora PK (1992) Microglial-produced nitric-oxide and reactive nitrogen-oxides mediate neuronal cell-death. Brain Res 587:250-256.
8. Brewer GJ (1997) Isolation and culture of adult rat hippocampal neurons. J Neurosci Methods 71:143-155.
9. Brown H, Kozlowski R, Perry H (1998) The importance of ion channels for macrophage and microglial activation in vitro. Glia 22:94-97.
10. Cahalan MD, Wulff H, Chandy KG (2001) Molecular properties and physiological roles of ion channels in the immune system. J Clin Immunol 21:235-252.
11. Cayabyab FS, Khanna R, Jones OT, Schlichter LC (2000) Suppression of the rat microglia Kv1.3 current by src-family tyrosine kinases and oxygen/glucose deprivation. Eur J Neurosci 12:1949-1960.
12. + channels as targets for specific immunomodulation. Trends Pharmacol Sci 25:280-289.
13. Chao CC, Hu SX, Molitor TW, Shaskan EG, Peterson PK (1992) Activated microglia mediate neuronal cell injury via a nitric-oxide mechanism. J Immunol 149:2736-2741.
14. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Bian J, Guo L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801.
15. Chung I, Schlichter LC (1997a) Native Kv1.3 channels are upregulated by protein kinase C. J Membr Biol 156:73-85.
16. Chung I, Schlichter LC (1997b) Regulation of native Kv1.3 channels by cAMP-dependent protein phosphorylation. Am J Physiol 273:C622-C633.
17. 2+ channels. Am J Physiol 266:C1650-C1655.
18. Dijkstra S, Geisert Jr EE, Dijkstra CD, Bar PR, Joosten EA (2001) CD81 and microglial activation in vitro: proliferation, phagocytosis and nitric oxide production. J Neuroimmunol 114:151-159.
19. Eder C (1998) Ion channels in microglia (brain macrophages). Am J Physiol 275:C327-C342.
20. + currents and ramification of brain macrophages. Neurosci Lett 226:147-150.
21. Evans MS, Collings MA, Brewer GJ (1998) Electrophysiology of embryonic, adult and aged rat hippocampal neurons in serum-free culture. J Neurosci Methods 79:37-46.
22. Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, Parsons AD, Overton JM, Koni PA, Flavell RA, Kaczmarek LK (2004) Kv1.3 channel gene-targeted deletion produces "Super-smeller mice" with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41:389-404.
23. Garcia ML, Hanner M, Knaus HG, Kach R, Schmalhofer W, Slaughter RS, Kaczorowski GJ (1997) Pharmacology of potassium channels. Adv Pharmacol 39:425-471.
24. Gebicke-Haerter PJ, 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.
25. Gehrmann J, Matsumoto Y, Kreutzberg GW (1995) Microglia: intrinsic immuneffector cell of the brain. Brain Res Brain Res Rev 20:269-287.
26. Gonzalez-Scarano F, Baituch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219-240.
27. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126:131-138.
28. + channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45:1227-1234.
29. Jeohn GH, Cooper CL, Jang KJ, Liu B, Lee DS, Kim HC, Hong JS (2002) Go6976 inhibits LPS-induced microglial TNFalpha release by suppressing p38 MAP kinase activation. Neuroscience 114:689-697.
30. + channels and the microglial espiratory burst. Am J Physiol Cell Physiol 280:C796-C806.
31. + channel blocker, in HepG2 human hepatoblastoma cells. Pharmacology 60:74-81.
32. Koistinaho M, Koistinaho J (2002) Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40:175-183.
33. Koo GC, Blake JT, Talento A, Nguyen M, Lin S, Sirotina A, Shah K, Mulvany K, Hora Jr D, Cunningham P, Wunderler DL, McManus OB, Slaughter R, Bugianesi R, Felix J, Garcia M, Williamson J, Kaczorowski GT, Sigal NH, Springer MS, et al. (1997) Blockade of the voltage-gated potassium channel Kv1.3 inhibits immune responses in vivo. J Immunol 158:5120-5128.
34. Kotecha SA, Schlichter LC (1999) A Kv1.5 to Kv1.3 switch in endogenous hippocampal microglia and a role in proliferation. J Neurosci 19:10680-10693.
35. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
36. Kues WA, Wunder F (1992) Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. Eur J Neurosci 4:1296-1308.
37. Lee SM, Yune TY, Kim SJ, Kim YC, Oh YJ, Markelonis GJ, Oh TH (2004) Minocycline inhibits apoptotic cell death via attenuation of TNF-α expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J Neurochem 91:568-578.
38. Lieb K, Engels S, Fiebich BL (2003) Inhibition of LPS-induced iNOS and NO synthesis in primary microglial cells. Neurochem Int 42:131-137.
39. Misko TP, Highkin MK, Veenhuizen AW, Manning PT, Stern MK, Currie MG, Salvemini D (1998) Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J Biol Chem 273:15646-15653.
40. Morimoto K, Murasugi T, Oda T (2002) Acute neuroinflammation exacerbates excitotoxicity in rat hippocampus in vivo. Exp Neurol 177:95-104.
41. Nakamura Y, Si QS, Kataoka K (1999) Lipopolysaccharide-induced microglial activation in culture: temporal profiles of morphological change and release of cytokines and nitric oxide. Neurosci Res 35:95-100.
42. Nelson PT, Soma LA, Lavi E (2002) Microglia in diseases of the central nervous system. Ann Med 34:491-500.
43. Norenberg W, Gebicke-Haerter PJ, Illes P (1994) Voltage-dependent potassium channels in activated rat microglia. J Physiol (Lond) 475:15-32.
44. Polazzi E, Contestabile A (2002) Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 13:221-242.
45. Pyo H, Chung S, Jou I, Gwag B, Joe EH (1997) Expression and function of outward K + channels induced by lipopolysaccharide in microglia. Mol Cells 7:610-614.
46. + channels and proliferation in neuroimmune cells. In: Roles of ion channels in physiopathology of nerve conduction and cell proliferation (Rouzaire-Dubois B, Benoit E, Dubois J-M, eds), pp 121-151. Karala, India: Research Signpost.
47. - channels and their involvement in proliferation of rat microglial cells. Glia 17:225-236.
48. Smith ME, van der MK, Somera FP, Sobel RA (1998) Effects of phorbol myristate acetate (PMA) on functions of macrophages and microglia in vitro. Neurochem Res 23:427-434.
49. 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.
50. Stollg G, Jander S (1999) The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 58:233-247.
51. Streit WJ (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40:133-139.
52. Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57:563-581.
53. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588.
54. van der Veen RC, Hinton DR, Incardonna F, Hofman FM (1997) Extensive peroxynitrite activity during progressive stages of central nervous system inflammation. J Neuroimmunol 77:1-7.
55. + channel profile of microglial cells. J Neurosci Res 47:233-241.
56. Wei L, Yu S-P, Gottron F, Snider J, Zipfel GJ, Choi DW (2003) Potassium blockers attenuate hypoxia- and ischemia-induced neuronal death in vitro and in vivo. Stroke 34:1281-1286.
57. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, Choi DK, Ischiropoulos H, Przedborski S (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 22:1763-1771.
58. Wulff H, Gutman GA, Chandy KG (2003) Potassium channels as therapeutic targets for autoimmune disorders. Curr Opin Drug Discov Devel 6:640-647.
59. 1-42- and lipopolysaccharide-activated microglia. J Neurosci 22:3484-3492.
60. Yong VW, Wells J, Giuliani F, Casha S, Power C, Metz LM (2004) The promise of minocycline in neurology. Lancet Neurol 3:744-751.
61. Zietlow R, Dunnett SB, Fawcett JW (1999) The effect of microglia on embryonic dopaminergic neuronal survival in vitro: diffusible signals from neurons and glia change microglia from neurotoxic to neuroprotective. Eur J Neurosci 11:1657-1667.