Regulation of Kv2.1 K+ conductance by cell surface channel density

Journal of Neuroscience

Volumn 33, Issue 3, 2013, Pages 1259-1270

  Fox, Philip D ^a   Loftus, Rob J ^a   Tamkun, Michael M ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL KV2.1; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FLUORESCENCE MICROSCOPY; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; LOCALIZATION; NONHUMAN; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VOLTAGE CLAMP;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MEMBRANE POTENTIALS; NEURONS; RATS; SHAB POTASSIUM CHANNELS;

EID: 84872356165     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3008-12.2013     Document Type: Article

References (48)

1. Amberg GC, Santana LF (2006) Kv2 channels oppose myogenic constriction of rat cerebral arteries. Am J Physiol Cell Physiol 291:C348-C356.CrossRef Medline
2. Baver SB, O'Connell KM (2012) The C-terminus of neuronal Kv2.1 channels is required for channel localization and targeting but not for NMDA-receptor-mediated regulation of channel function. Neuroscience 217:56-66. CrossRef Medline
3. Coppock EA, Tamkun MM (2001) Differential expression of K(V) channel -and -subunits in the bovine pulmonary arterial circulation. Am J Physiol Heart Circ Physiol 281:L1350-L1360. Medline
4. Dallas ML, Boyle JP, Milligan CJ, Sayer R, Kerrigan TL, McKinstry C, Lu P, Mankouri J, Harris M, Scragg JL, Pearson HA, Peers C (2011) Carbon monoxide protects against oxidant-induced apoptosis via inhibition of Kv2.1. FASEB J 25:1519-1530. CrossRef Medline
5. Deutsch E, Weigel AV, Akin EJ, Fox P, Hansen G, Haberkorn CJ, Loftus R, Krapf D, Tamkun MM (2012) Kv2.1 cell surface clusters are insertion platforms for ion channel delivery to the plasma membrane. Mol Biol Cell 23:2917-2929. CrossRef Medline
6. Du J, Haak LL, Phillips-Tansey E, Russell JT, McBain CJ (2000) Frequency- dependent regulation of rat hippocampal somato-dendritic excitability by the K channel subunit Kv2.1. J Physiol 522:19-31. CrossRef Medline
7. Feinshreiber L, Singer-Lahat D, Friedrich R, Matti U, Sheinin A, Yizhar O, Nachman R, Chikvashvili D, Rettig J, Ashery U, Lotan I (2010) Nonconducting function of the Kv2.1 channel enables it to recruit vesicles for release in neuroendocrine and nerve cells. J Cell Sci 123:1940-1947.CrossRef Medline
8. Fujiwara Y, Kubo Y (2004) Density-dependent changes of the pore proper ties of the P2X2 receptor channel. J Physiol 558:31-43. CrossRef Medline
9. Gentet LJ, Stuart GJ, Clements JD (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 79:314-320. CrossRef Medline
10. Guan D, Tkatch T, Surmeier DJ, Armstrong WE, Foehring RC (2007) Kv2 subunits underlie slowly inactivating potassium current in rat neocortical pyramidal neurons. J Physiol 581:941-960. CrossRef Medline
11. Guan D, Horton LR, Armstrong WE, Foehring RC (2011) Postnatal development of A-type and Kv1- and Kv2-mediated potassium channel currents in neocortical pyramidal neurons. J Neurophysiol 105:2976-2988.CrossRef Medline
12. Guillemare E, Honoré E, Pradier L, Lesage F, Schweitz H, Attali B, Barhanin J, Lazdunski M (1992) Effects of the level of mRNA expression on biophysical properties, sensitivity to neurotoxins, and regulation of the brain delayed-rectifier K channels Kv1.2. Biochemistry 31:12463-12468.CrossRef Medline
13. Honoré E, Attali B, Romey G, Lesage F, Barhanin J, Lazdunski M (1992) Different types of K channel current are generated by different levels of a single mRNA. EMBO J 11:2465-2471. Medline
14. Hulme JT, Coppock EA, Felipe A, Martens JR, Tamkun MM (1999) Oxygen sensitivity of cloned voltage-gated K channels expressed in the pulmonary vasculature. Circ Res 85:489-497. CrossRef Medline
15. Immke D, Wood M, Kiss L, Korn SJ (1999) Potassium-dependent changes in the conformation of the Kv2.1 potassium channel pore. J Gen Physiol 113:819-836. CrossRef Medline
16. Islas LD, Sigworth FJ (1999) Voltage sensitivity and gating charge in Shaker and Shab family potassium channels. J Gen Physiol 114:723-742.CrossRef Medline
17. Kihira Y, Hermanstyne TO, Misonou H (2010) Formation of heteromeric Kv2 channels in mammalian brain neurons. J Biol Chem 285: 15048-15055. CrossRef Medline
18. Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178-186. CrossRef Medline
19. Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355-358. CrossRef Medline
20. Lim ST, Antonucci DE, Scannevin RH, Trimmer JS (2000) A novel targeting signal for proximal clustering of the Kv2.1 K channel in hippocampal neurons. Neuron 25:385-397. CrossRef Medline
21. Malin SA, Nerbonne JM (2002) Delayed rectifier K currents, IK, are encoded by Kv2 alpha-subunits and regulate tonic firing in mammalian sympathetic neurons. J Neurosci 22:10094-10105. Medline
22. Manganas LN, Trimmer JS (2000) Subunit composition determines Kv1 potassium channel surface expression. J Biol Chem 275:29685-29693.CrossRef Medline
23. Mashanov GI, Tacon D, Knight AE, Peckham M, Molloy JE (2003) Visualizing single molecules inside living cells using total internal reflection fluorescence microscopy. Methods 29:142-152. CrossRef Medline
24. Misonou H, Mohapatra DP, Park EW, Leung V, Zhen D, Misonou K, Anderson AE, Trimmer JS (2004) Regulation of ion channel localization and phosphorylation by neuronal activity. Nat Neurosci 7:711-718. CrossRef Medline
25. Misonou H, Mohapatra DP, Menegola M, Trimmer JS (2005) Calcium- and metabolic state-dependent modulation of the voltage-dependent Kv2.1 channel regulates neuronal excitability in response to ischemia. J Neurosci 25:11184-11193. CrossRef Medline
26. Misonou H, Thompson SM, Cai X (2008) Dynamic regulation of the Kv2.1 voltage-gated potassium channel during brain ischemia through neuroglial interaction. J Neurosci 28:8529-8538. CrossRef Medline
27. Mohapatra DP, Trimmer JS (2006) The Kv2.1 C terminus can autonomously transfer Kv2.1-like phosphorylation-dependent localization, voltage-dependent gating, and muscarinic modulation to diverse Kv channels. J Neurosci 26:685-695. CrossRef Medline
28. Mohapatra DP, Siino DF, Trimmer JS (2008) Interdomain cytoplasmic in- teractions govern the intracellular trafficking, gating, and modulation of the Kv2.1 channel. J Neurosci 28:4982-4994. CrossRef Medline
29. Mulholland PJ, Carpenter-Hyland EP, Hearing MC, Becker HC, Woodward JJ, Chandler LJ (2008) Glutamate transporters regulate extrasynaptic NMDA receptor modulation of Kv2.1 potassium channels. J Neurosci 28:8801-8809. CrossRef Medline
30. Murakoshi H, Trimmer JS (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. Medline
31. O'Connell KM, Tamkun MM (2005) Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J Cell Sci 118: 2155-2166. CrossRef Medline
32. O'Connell KM, Rolig AS, Whitesell JD, Tamkun MM (2006) Kv2.1 potassium channels are retained within dynamic cell surface microdomains that are defined by a perimeter fence. J Neurosci 26:9609-9618. CrossRef Medline
33. O'Connell KM, Loftus R, Tamkun MM (2010) Localization-dependent ac- tivity of the Kv2.1 delayed-rectifier K channel. Proc Natl Acad Sci U S A 107:12351-12356. CrossRef Medline
34. Pardo LA, Heinemann SH, Terlau H, Ludewig U, Lorra C, Pongs O, Stuhmer W (1992) Extracellular K specifically modulates a rat brain K channel. Proc Natl Acad Sci U S A 89:2466-2470. CrossRef Medline
35. Park KS, Mohapatra DP, Misonou H, Trimmer JS (2006) Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 313: 976-979. CrossRef Medline
36. Plant LD, Dowdell EJ, Dementieva IS, Marks JD, Goldstein SA (2011) SUMO modification of cell surface Kv2.1 potassium channels regulates the activity of rat hippocampal neurons. J Gen Physiol 137:441-454.CrossRef Medline
37. Scannevin RH, Murakoshi H, Rhodes KJ, Trimmer JS (1996) Identification of a cytoplasmic domain important in the polarized expression and clustering of the Kv2.1 K channel. J Cell Bio 135:1619-1632. CrossRef Medline
38. Shaw G, Morse S, Ararat M, Graham FL (2002) Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16:869-871. CrossRef Medline
39. Shi G, Kleinklaus AK, Marrion NV, Trimmer JS (1994) Properties of Kv2.1 K channels expressed in transfected mammalian cells. J Biol Chem 269: 23204-23211. Medline
40. Singer-Lahat D, Sheinin A, Chikvashvili D, Tsuk S, Greitzer D, Friedrich R, Feinshreiber L, Ashery U, Benveniste M, Levitan ES, Lotan I (2007) K channel facilitation of exocytosis by dynamic interaction with syntaxin. J Neurosci 27:1651-1658. CrossRef Medline
41. Stuhmer W, Ruppersberg JP, Schröter 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. Medline
42. Sugiyama Y, Kawabata I, Sobue K, Okabe S (2005) Determination of absolute protein numbers in single synapses by a GFP-based calibration technique. Nat Methods 2:677-684. CrossRef Medline
43. Tamkun MM, O'Connell KM, Rolig AS (2007) A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels. J Cell Sci 120:2413-2423. CrossRef Medline
44. Trapani JG, Andalib P, Consiglio JF, Korn SJ (2006) Control of single channel conductance in the outer vestibule of the Kv2.1 potassium channel. J Gen Physiol 128:231-246. CrossRef Medline
45. Tseng-Crank J, Yao JA, Berman MF, Tseng GN (1993) Functional role of the NH2-terminal cytoplasmic domain of a mammalian A-type K channel. J Gen Physiol 102:1057-1083. CrossRef Medline
46. Ulbrich MH, Isacoff EY (2007) Subunit counting in membrane-bound proteins. Nat Methods 4:319-321. CrossRef Medline
47. Weigel AV, Simon B, Tamkun MM, Krapf D (2011) Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. Proc Natl Acad Sci U S A 108:6438-6443. CrossRef Medline
48. Yang J, Thio LL, Clifford DB, Zorumski CF (1993) Electrophysiological properties of identified postnatal rat hippocampal pyramidal neurons in primary culture. Brain Res Dev Brain Res 71:19-26. CrossRef Medline