Interdomain cytoplasmic interactions govern the intracellular trafficking, gating, and modulation of the Kv2.1 channel

Journal of Neuroscience

Volumn 28, Issue 19, 2008, Pages 4982-4994

  Mohapatra, Durga P ^a   Siino, Dominic F ^a   Trimmer, James S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Assembly; Electrophysiology; Hippocampal neurons; Immunocytochemistry; Phosphorylation; Potassium channel

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; PROTEIN KV2.1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; SHAB POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; ANIMAL; CELL LINE; CELL MEMBRANE; CERCOPITHECUS; CHANNEL GATING; ELECTROPHYSIOLOGY; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RAT;

AMINO ACID MOTIFS; ANIMALS; CELL LINE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CYTOPLASM; ELECTROPHYSIOLOGY; HUMANS; INTRACELLULAR MEMBRANES; ION CHANNEL GATING; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; SHAB POTASSIUM CHANNELS;

EID: 44949210432     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0186-08.2008     Document Type: Article

References (76)

1. Adair B, Nunn R, Lewis S, Dukes I, Philipson L, Yeager M (2008) Single particle image reconstruction of the human recombinant Kv2.1 channel. Biophys J 94:2106-2114.
2. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, Rhodes KJ (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403:553-556.
3. Antonucci DE, Lim ST, Vassanelli S, Trimmer JS (2001) Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108:69-81.
4. Bahring R, Dannenberg J, Peters HC, Leicher T, Pongs O, Isbrandt D (2001) Conserved Kv4 N-terminal domain critical for effects of Kv channel-interacting protein 2.2 on channel expression and gating. J Biol Chem 276:23888-23894.
5. Bentley GN, Brooks MA, O'Neill CA, Findlay JB (1999) Determinants of potassium channel assembly localised within the cytoplasmic C-terminal domain of Kv2.1. Biochim Biophys Acta 1418:176-184.
6. + channels. Nat Struct Biol 6:38-43.
7. Campomanes CR, Carroll KI, Manganas LN, Hershberger ME, Gong B, Antonucci DE, Rhodes KJ, Trimmer JS (2002) Kv beta subunit oxidoreductase activity and Kv1 potassium channel trafficking. J Biol Chem 277:8298-8305.
8. Chung JJ, Li M (2005) Biochemical characterization of the native Kv2.1 potassium channel. FEBS J 272:3743-3755.
9. + channel subunit Kv2.1. J Physiol (Lond) 522:19-31.
10. Gong J, Xu J, Bezanilla M, van Huizen R, Derin R, Li M (1999) Differential stimulation of PKC phosphorylation of potassium channels by ZIP1 and ZIP2. Science 285:1565-1569.
11. Gordon SE, Varnum MD, Zagotta WN (1997) Direct interaction between amino- and carboxyl-terminal domains of cyclic nucleotide-gated channels. Neuron 19:431-441.
12. Gu C, Jan YN, Jan LY (2003) A conserved domain in axonal targeting of Kv1 (Shaker) voltage-gated potassium channels. Science 301:646-649.
13. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
14. + channels. Science 289:123-127.
15. Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D, Pardo LA, Robertson GA, Rudy B, Sanguinetti MC, Stuhmer W, Wang X (2005) International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 57:473-508.
16. + channels of the Shab subfamily. J Neurosci 13:1569-1576.
17. Ikemoto N, Yamamoto T (2002) Regulation of calcium release by interdomain interaction within ryanodine receptors. Front Biosci 7:d671-d683.
18. Jerng HH, Pfaffinger PJ, Covarrubias M (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27:343-369.
19. Ju M, Stevens L, Leadbitter E, Wray D (2003) The roles of N- and C-terminal determinants in the activation of the Kv2.1 potassium channel. J Biol Chem 278:12769-12778.
20. Kobrinsky E, Stevens L, Kazmi Y, Wray D, Soldatov NM (2006) Molecular rearrangements of the Kv2.1 potassium channel termini associated with voltage gating. J Biol Chem 281:19233-19240.
21. Kreusch A, Pfaffinger PJ, Stevens CF, Choe S (1998) Crystal structure of the tetramerization domain of the Shaker potassium channel. Nature 392:945-948.
22. Li M, Jan YN, Jan LY (1992) Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel. Science 257:1225-1230.
23. Li Y, Um SY, McDonald TV (2006) Voltage-gated potassium channels: regulation by accessory subunits. Neuroscientist 12:199-210.
24. + channel in hippocampal neurons. Neuron 25:385-397.
25. + channel. Science 309:897-903.
26. + currents, IK, are encoded by Kv2 alpha-subunits and regulate tonic firing in mammalian sympathetic neurons. J Neurosci 22:10094-10105.
27. Manganas LN, Trimmer JS (2000) Subunit composition determines Kv1 potassium channel surface expression. J Biol Chem 275:29685-29693.
28. Manganas LN, Wang Q, Scannevin RH, Antonucci DE, Rhodes KJ, Trimmer JS (2001a) Identification of a trafficking determinant localized to the Kv1 potassium channel pore. Proc Natl Acad Sci USA 98:14055-14059.
29. Manganas LN, Akhtar S, Antonucci DE, Campomanes CR, Dolly JO, Trimmer JS (2001b) Episodic ataxia type-1 mutations in the Kv1.1 potassium channel display distinct folding and intracellular trafficking properties. J Biol Chem 276:49427-49434.
30. Minor DL, Lin YF, Mobley BC, Avelar A, Jan YN, Jan LY, Berger JM (2000) The polar T1 interface is linked to conformational changes that open the voltage-gated potassium channel. Cell 102:657-670.
31. 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.
32. 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.
33. Misonou H, Menegola M, Mohapatra DP, Guy LK, Park KS, Trimmer JS (2006) Bidirectional activity-dependent regulation of neuronal ion channel phosphorylation. J Neurosci 26:13505-13514.
34. 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.
35. + current in rat hippocampal neurons. J Neurosci 19:1728-1735.
36. + channel alters voltage-dependent activation. Mol Pharmacol 52:821-828.
37. Nanao MH, Zhou W, Pfaffinger PJ, Choe S (2003) Determining the basis of channel-tetramerization specificity by x-ray crystallography and a sequence-comparison algorithm: Family Values (FamVal). Proc Natl Acad Sci USA 100:8670-8675.
38. Naren AP, Cormet-Boyaka E, Fu J, Villain M, Blalock JE, Quick MW, Kirk KL (1999) CFTR chloride channel regulation by an interdomain interaction. Science 286:544-548.
39. Nishida M, MacKinnon R (2002) Structural basis of inward rectification: cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8 A resolution. Cell 111:957-965.
40. O'Connell KM, Tamkun MM (2005) Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J Cell Sci 118:2155-2166.
41. 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.
42. Papazian DM (1999) Potassium channels: some assembly required. Neuron 23:7-10.
43. Park KS, Mohapatra DP, Misonou H, Trimmer JS (2006) Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 313:976-979.
44. Park KS, Mohapatra DP, Trimmer JS (2007) Proteomic analyses of Kv2.1 channel phosphorylation sites determining cell background-specific differences in function. Channels 1:59-61.
45. Pegan S, Arrabit C, Zhou W, Kwiatkowski W, Collins A, Slesinger PA, Choe S (2005) Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification. Nat Neurosci 8:279-287.
46. + channel T1 domain self-tetramerizes to a stable structure. J Biol Chem 270:28595-28600.
47. Pongs O (1999) Voltage-gated potassium channels: from hyperexcitability to excitement. FEBS Lett 452:31-35.
48. + channel α- and β-subunit polypeptides in rat brain. J Neurosci 15:5360-5371.
49. Rhodes KJ, Carroll KI, Sung MA, Doliveira LC, Monaghan MM, Burke SL, Strassle BW, Buchwalder L, Menegola M, Cao J, An WF, Trimmer JS (2004) KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. J Neurosci 24:7903-7915.
50. + channel. J Cell Biol 135:1619-1632.
51. Scannevin RH, Wang K, Jow F, Megules J, Kopsco DC, Edris W, Carroll KC, Lü Q, Xu W, Xu Z, Katz AH, Olland S, Lin L, Taylor M, Stahl M, Malakian K, Somers W, Mosyak L, Bowlby MR, Chanda P, et al. (2004) Two N-terminal domains of Kv4 K(+) channels regulate binding to and modulation by KChIP1. Neuron 41:587-598.
52. Scholle A, Zimmer T, Koopmann R, Engeland B, Pongs O, Benndorf K (2004) Effects of Kv1.2 intracellular regions on activation of Kv2.1 channels. Biophys J 87:873-882.
53. Schrader LA, Anderson AE, Mayne A, Pfaffinger PJ, Sweatt JD (2002) PKA modulation of Kv4.2-encoded A-type potassium channels requires formation of a supramolecular complex. J Neurosci 22:10123-10133.
54. + channels. Biochemistry 35:12133-12140.
55. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381-3385.
56. Sewing S, Roeper J, Pongs O (1996) Kv beta 1 subunit binding specific for shaker-related potassium channel alpha subunits. Neuron 16:455-463.
57. + channels in PC12 cells. J Cell Biol 123:1835-1843.
58. + channel surface expression through effects early in biosynthesis. Neuron 16:843-852.
59. Shibata R, Misonou H, Campomanes CR, Anderson AE, Schrader LA, Doliveira LC, Carroll KI, Sweatt JD, Rhodes KJ, Trimmer JS (2003) A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels. J Biol Chem 278:36445-36454.
60. + channel facilitation of exocytosis by dynamic interaction with syntaxin. J Neurosci 27:1651-1658.
61. Singer-Lahat D, Chikvashvili D, Lotan I (2008) Direct interaction of endogenous kv channels with syntaxin enhances exocytosis by neuroendocrine cells. PLoS ONE 3:e1381.
62. Sun W, Barchi RL, Cohen SA (1995) Probing sodium channel cytoplasmic domain structure. Evidence for the interaction of the rSkM1 amino and carboxyl termini. J Biol Chem 270:22271-22276.
63. 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.
64. + channel surface expression and clustering. J Cell Biol 148:147-158.
65. Tombola F, Pathak MM, Isacoff EY (2006) How does voltage open an ion channel? Annu Rev Cell Dev Biol 22:23-52.
66. + channel polypeptide in rat brain. Proc Natl Acad Sci USA 88:10764-10768.
67. Tsuk S, Michaelevski I, Bentley GN, Joho RH, Chikvashvili D, Lotan I (2005) Kv2.1 channel activation and inactivation is influenced by physical interactions of both syntaxin 1A and the syntaxin 1A/soluble N-ethylmaleimide-sensitive factor-25 (t-SNARE) complex with the C terminus of the channel. Mol Pharmacol 67:480-488.
68. Vacher H, Misonou H, Trimmer JS (2006) Determinants of voltage-gated potassium channel distribution in mammalian neurons. In: Protein trafficking in neurons (Bean AJ, ed), pp 244-270. London: Elsevier Academic.
69. + channel function by deletions at the N- and C-termini. Neuron 5:433-443.
70. Varnum MD, Zagotta WN (1997) Interdomain interactions underlying activation of cyclic nucleotide-gated channels. Science 278:110-113.
71. + channels by auxiliary KChIP subunits. Nat Neurosci 10:32-39.
72. Yang JW, Vacher H, Park KS, Clark E, Trimmer JS (2007) Trafficking-dependent phosphorylation of Kv1.2 regulates voltage-gated potassium channel cell surface expression. Proc Natl Acad Sci USA 104:20055-20060.
73. Yu W, Xu J, Li M (1996) NAB domain is essential for the subunit assembly of both alpha-alpha and alpha-beta complexes of shaker-like potassium channels. Neuron 16:441-453.
74. Zerangue N, Schwappach B, Jan YN, Jan LY (1999) A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22:537-548.
75. 2+-calmodulin modulation of cyclic nucleotide-gated channels. J Neurosci 23:8167-8175.
76. + channels. Neuron 41:573-586.