KCNQ2 Is a Nodal K+ Channel

Journal of Neuroscience

Volumn 24, Issue 5, 2004, Pages 1236-1244

  Devaux, Jérôme J ^a   Kleopa, Kleopas A ^a,b   Cooper, Edward C ^a   Scherer, Steven S ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

Author keywords

Epilepsy; Kv; M current; Myelin; Neuromyotonia; Potassium channel; Repolarization

Indexed keywords

ANKYRIN; KCNQ2 PROTEIN; LINOPIRDINE; MEMBRANE PROTEIN; POTASSIUM CHANNEL; RETIGABINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPILEPSY; EPILEPTOGENESIS; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; MYOKYMIA; NERVE CELL EXCITABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RANVIER NODE; RAT; REGULATORY MECHANISM; REPOLARIZATION;

AMINO ACID SUBSTITUTION; ANIMALS; ANKYRINS; BRAIN; HELA CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MICE; MUTATION; MYOKYMIA; OPTIC NERVE; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; PRECIPITIN TESTS; RANVIER'S NODES; RATS; RATS, WISTAR; SCIATIC NERVE; SPINAL CORD;

EID: 0842346580     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4512-03.2004     Document Type: Article

References (70)

1. Arroyo EJ, Scherer SS (2000) On the molecular architecture of myelinated fibers. Histochem Cell Biol 113:1-18.
2. Arroyo EJ, Xu Y-T, Zhou L, Messing A, Peles E, Chiu SY, Scherer SS (1999) Myelinating Schwann cells determine the internodal localization of Kv1.1, Kv1.2, Kvβ2, and Caspr. J Neurocytol 28:333-347.
3. Arroyo EJ, Xu T, Poliak S, Watson M, Peles E, Scherer SS (2001) Internodal specializations of myelinated axons in the CNS. Cell Tissue Res 305:53-66.
4. Arroyo EJ, Xu T, Grinspan J, Lambert S, Levinson SR, Brophy PJ, Peles E, Scherer SS (2002) Genetic dysmyelination alters the molecular architecture of the nodal region. J Neurosci 22:1726-1737.
5. Auger RG, Daube JR, Gomez MR, Lambert EH (1984) Hereditary form of sustained muscle activity of peripheral nerve origin causing generalized myokymia and muscle stiffness. Ann Neurol 15:13-21.
6. Bartsch S, Bartsch U, Dorries U, Faissner A, Weller A, Ekblom P, Schachner M (1992) Expression of tenascin in the developing and adult cerebellar cortex. J Neurosci 12:736-749.
7. Bennett V, Chen L (2001) Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr Opin Cell Biol 13:61-67.
8. Bergmann C, Nonner W, Stampfli R (1968) Sustained spontaneous activity of Ranvier nodes induced by the combined actions of TEA and lack of calcium. Pflügers Arch 302:24-37.
9. Bouzidi M, Tricaud N, Giraud P, Kordeli E, Caillol G, Deleuze C, Couraud F, Alcaraz G (2002) Interaction of the Nav1.2a subunit of the voltagedependent sodium channel with nodal AnkyrinG: in vitro mapping of the interacting domains and association in synaptosomes. J Biol Chem 277:28996-29004.
10. Browne DL, Gancher ST, Nutt JG, Brunt ERP, Smith EA, Kramer P, Litt M (1994) Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet 8:136-140.
11. Castaldo P, del Giudice EM, Coppola G, Pascotto A, Annunziato L, Taglialatela M (2002) Benign familial neonatal convulsions caused by altered gating of KCNQ2/KCNQ3 potassium channels. J Neurosci 22:RC199(1-6).
12. + channels. Ann NY Acad Sci 868:233-285.
13. Conradi S (1969) Observations on the ultrastructure of the axon hillock and initial segment of lumbosacral motoneurons in the cat. Acta Physiol Scand [Suppl] 332:65-92.
14. Cooper EC, Aldape KD, Abosch A, Barbaro NM, Berger MS, Peacock WS Jan YN, Jan LY (2000) Colocalization and coassembly of two human brain M-type potassium channel subunits that are mutated in epilepsy. Proc Natl Acad Sci USA 97:4914-4919.
15. Cooper EC, Harrington E, Jan YN, Jan LY (2001) M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J Neurosci 21:9529-9540.
16. + channels in rat myelinated fibres and their sensitivity to dendrotoxin. Pfügers Arch 418:408-416.
17. + channel. Proc Natl Acad Sci USA 98:12272-12277.
18. + channels. J Neurophysiol 87:1376-1385.
19. Devaux J, Alcaraz G, Grinspan J, Bennett V, Joho R, Crest M, Scherer SS (2003) Kv3.1b is a novel component of CNS nodes. J Neurosci 23:4509-4518.
20. Dubois JM (1981) Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane. J Physiol (Lond) 318:297-316.
21. Dubois JM (1983) Potassium currents in the frog node of Ranvier. Prog Biophys Mol Biol 42:1-20.
22. Eng DL, Gordon TR, Kocsis JD, Waxman SG (1988) Development of 4-AP and TEA sensitivities in mammalian myelinated nerve fibers. J Neurophysiol 60:2168-2179.
23. Eunson LH, Rea R, Zuberi SM, Youroukos S, Panayiotopoulos CP, Liguori R, Avoni P, McWilliam RC, Stephenson JBP, Hanna MG, Kullmann DM, Spauschus A (2000) Clinical, genetic, and expression studies of mutations in the potassium channel gene KCNA1 reveal new phenotypic variability. Ann Neurol 48:647-656.
24. Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL, Colman DR (1995) Novel E-cadherin mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions. J Cell Biol 129:189-202.
25. ffrench-Constant C, Miller RH, Kruse J, SchachnerM, Raff MC (1986) Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve. J Cell Biol 102:844-852.
26. Gutmann L, Libell D, Gutmann L (2001) When is myokymia neuromyotonia? Muscle Nerve 24:151-153.
27. Hartshorne RP, Catterall WA (1984) The sodium channel from rat brain. Purification and subunit composition. J Biol Chem 259:1667-1675.
28. + currents expressed in Xenopus oocytes by mKv1.1, mKv1.2 and their heteromultimers as revealed by mutagenesis of the dendrotoxin-binding site in Kv1.1. Pflügers Arch 428:382-390.
29. Jenkins SM, Bennett V (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and LI CAMs at Purkinje neuron initial segments. J Cell Biol 155:739-746.
30. Jenkins SM, Bennett V (2002) Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc Natl Acad Sci USA 99:2303-2308.
31. Jenkins SM, Kizhatil K, Kramarcy NR, Sen A, Sealock R, Bennett V (2001) FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons. J Cell Sci 114:3823-3835.
32. Jentsch TJ (2000) Neuronal KCNQ potassium channels: physiology and role in disease. Nat Rev Neurosci 1:21-30.
33. + channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Natl Acad Sci USA 97:4333-4338.
34. Komada M, Soriano P (2002) Beta IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 156:337-348.
35. G: a new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 270:2352-2359.
36. Lee V, Wu HL, Schlaepfer WW (1982) Monoclonal antibodies recognized individual neurofilament triplet proteins. Proc Natl Acad Sci USA 79:6089-6092.
37. Lee VM-Y, Carden MJ, Schlaepfer WW, Trojanowski JQ (1987) Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats. J Neurosci 7:3474-3488.
38. Malhotra JD, Koopmann MC, Kazen-Gillespie KA, Fettman N, Hortsch M, Isom LL (2002) Structural requirements for interaction of sodium channel beta 1 subunits with ankyrin. J Biol Chem 277:26681-26688.
39. Mi HY, Deerinck TJ, Ellisman MH, Schwarz TL (1995) Differential distribution of closely related potassium channels in rat Schwann cells. J Neurosci 15:3761-3774.
40. Newsom-Davis J (1997) Autoimmune neuromyotonia (Isaacs' syndrome): an antibody-mediated potassium channelopathy. Ann NY Acad Sci 835:111-119.
41. Pan Z, Selyanko AA, Hadley JK, Brown DA, Dixon JE, McKinnon D (2001) Alternative splicing of KCNQ2 potassium channel transcripts contributes to the functional diversity of M-currents. J Physiol (Lond) 531:347-358.
42. Peles E, Salzer JL (2000) Molecular domains of myelinated fibers. Curr Opin Neurobiol 10:558-565.
43. Rasband MN, Trimmer JS (2001) Developmental clustering of ion channels at and near the node of Ranvier. Dev Biol 236:5-16.
44. Robbins J (2001) KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharmacol Ther 90:1-19.
45. + channels. Br J Pharmacol 137:1173-1186.
46. Roper J, Schwarz JR (1989) Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. J Physiol (Lond) 416:93-110.
47. Rorke LB, Riggs HE (1969) Myelination of the brain in the newborn. Philadelphia: Lippincott.
48. + channel opening effect of the anticonvulsant retigabine in PC12 cells. Epilepsy Res 35:99-107.
49. Rundfeldt C, Netzer R (2000) The novel anticonvulsant retigabine activates M-currents in Chinese hamster ovary cells tranfected with human KCNQ2/3 subunits. Neurosci Lett 282:73-76.
50. Safronov BV, Kampe K, Vogel W (1993) Single voltage-dependent potassium channels in rat peripheral nerve membrane. J Physiol (Lond) 460:675-691.
51. Scherer SS, Arroyo EJ (2002) Recent progress on the molecular organization of myelinated axons. J Periph Nerv Syst 7:1-12.
52. + channels causes epilepsy. Nature 396:687-690.
53. Selyanko AA, Hadley JK, Wood IC, Abogadie FC, Jentsch TJ, Brown DA (2000) Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J Physiol (Lond) 522 3:349-355.
54. Shah MM, Mistry M, Marsh SJ, Brown DA, Delmas P (2002) Molecular correlates of the M-current in cultured rat hippocampal neurons. J Physiol (Lond) 544:29-37.
55. Shapiro MS, Roche JP, Kaftan EJ, Cruzblanca H, Mackie K, Hille B (2000) Reconstitution of muscarinic modulation of the KCNQ2/KCNQ3(+) channels that underlie the neuronal M current. J Neurosci 20:1710-1721.
56. + channels of peripheral nerves. Ann Neurol 38:714-722.
57. Smart SL, Lopantsev V, Zhang CL, Robbins CA, Wang H, Chiu SY, Schwartzkroin PA, Messing A, Tempel BL (1998) Deletion of the Kv1.1 potassium channel causes epilepsy in mice. Neuron 20:809-819.
58. Smith JS, Iannotti CA, Dargis P, Christian EP, Aiyar J (2001) Differential expression of KCNQ2 splice variants: implications to M current function during neuronal development. J Neurosci 21:1096-1103.
59. Tatulian L, Delmas P, Abogadie FC, Brown DA (2001) Activation of expressed KCNQ potassium currents and native neuronal M-type potassium currents by the anti-convulsant drug retigabine. J Neurosci 21:5535-5545.
60. Vabnick I, Trimmer JS, Schwarz TL, Levinson SR, Risal D, Shrager P (1999) Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J Neurosci 19:747-758.
61. Vincent A (2000) Understanding neuromyotonia. Muscle Nerve 23:655-657.
62. + channels in terminal and juxtaparanodal regions of neurons. Nature 365:75-79.
63. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, McKinnon D (1998) KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282:1890-1893.
64. Wen H, Levitan IB (2002) Calmodulin is an auxiliary subunit of KCNQ2/3 potassium channels. J Neurosci 22:7991-8001.
65. Winckler B, Forscher P, Melman I (1999) A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397:698-701.
66. Yus-Najera A, Munoz A, Salvador N, Jensen BS, Rasmussen HB, Defelipe J, Villarroel A (2003) Localization of KCNQ5 in the normal and epileptic human temporal neocortex and hippocampal formation. Neuroscience 120:353-364.
67. Zerr P, Adelman JP, Maylie J (1998) Episodic ataxia mutations in Kv1.1 alter potassium channel function by dominant negative effects or haploin sufficiency. J Neurosci 18:2842-2848.
68. G is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143:1295-1304.
69. Zhou L, Messing A, Chiu SY (1999) Determinants of excitability at transition zones in Kv1.1-deficient myelinated nerves. J Neurosci 19:5768-5781.
70. Zuberi SM, Eunson LH, Spauschus A, De Silva R, Tolmie J, Wood NW, McWilliam RC, Stephenson JP, Kullmann DM, Hanna MG (1999) A novel mutation in the human voltage-gated potassium channel gene (Kv1.1) associates with episodic ataxia type 1 and sometimes with partial epilepsy. Brain 122:817-825.