A common ankyrin-G-based mechanism retains KCNQ and Na V channels at electrically active domains of the axon

Journal of Neuroscience

Volumn 26, Issue 10, 2006, Pages 2599-2613

  Pan, Zongming ^a   Kao, Tingching ^a   Horvath, Zsolt ^a   Lemos, Julia ^a   Sul, Jai Yoon ^a   Cranstoun, Stephen D ^b   Bennett, Vann ^c   Scherer, Steven S ^a   Cooper, Edward C ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Action potential; Axon initial segment; Epilepsy; M current; Neuromodulation; Node of Ranvier

Indexed keywords

ACTIN; AMINO ACID; ANKYRIN; ANTIBODY; CELL ADHESION MOLECULE; EPITOPE; MEMBRANE PROTEIN; POTASSIUM CHANNEL KCNQ1; SODIUM CHANNEL; SPECTRIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPILEPSY; FLUORESCENCE; GENE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; MOUSE; NERVE FIBER; NEUROMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANVIER NODE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANKYRINS; AXONS; BLOTTING, WESTERN; CELLS, CULTURED; EMBRYO; EVOLUTION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, MOLECULAR; MOLECULAR BIOLOGY; NEURONS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RANVIER'S NODES; RATS; SODIUM CHANNELS; TIME FACTORS; TRANSFECTION;

EID: 33644819526     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4314-05.2006     Document Type: Article

References (95)

1. Adelman JP, Bond CT, Pessia M, Maylie J (1995) Episodic ataxia results from voltage-dependent potassium channels with altered functions. Neuron 15:1449-1454.
2. Anderson WA, Flumerfelt BA (1984) Time course of mossy fiber degeneration following pontine ablation in the rat. J Comp Neurol 227:401-413.
3. Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81:1353-1392.
4. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK (1998) A potassium channel mutation in neonatal human epilepsy. Science 279:403-406.
5. Brown D (1988) M-currents: an update. Trends Neurosci 11:294-299.
6. + current in a vertebrate neuron. Nature 283:673-676.
7. Buchhalter JR, Dichter MA (1991) Electrophysiological comparison of pyramidal and stellate nonpyramidal neurons in dissociated cell culture of rat hippocampus. Brain Res Bull 26:333-338.
8. Bullock TH, Moore JK, Fields RD (1984) Evolution of myelin sheaths: both lamprey and hagfish lack myelin. Neurosci Lett 48:145-148.
9. Burke D, Kiernan MC, Bostock H (2001) Excitability of human axons. Clin Neurophysiol 112:1575-1585.
10. Chang SH, Low PS (2003) Identification of a critical ankyrin-binding loop on the cytoplasmic domain of erythrocyte membrane band 3 by crystal structure analysis and site-directed mutagenesis. J Biol Chem 278:6879-6884.
11. Chan-Palay V (1972) The tripartite structure of the undercoat in initial segments of Purkinje cell axons. Z Anat Entwicklungsgesch 139:1-10.
12. Chiu SY, Ritchie JM, Rogart RB, Stagg D (1979) A quantitative description of membrane currents in rabbit myelinated nerve. J Physiol (Lond) 292:149-166.
13. Coombs JS, Curtis DR, Eccles JC (1957) The generation of impulses in motoneurones. J Physiol (Lond) 139:232-249.
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. + channel. Proc Natl Acad Sci USA 98:12272-12277.
17. + channel. J Neurosci 24:1236-1244.
18. Doolittle RF (1994) Convergent evolution: the need to be explicit. Trends Biochem Sci 19:15-18.
19. Dubois JM (1983) Potassium currents in the frog node of Ranvier. Prog Biophys Mol Biol 42:1-20.
20. Fache MP, Moussif A, Fernandes F, Giraud P, Garrido JJ, Dargent B (2004) Endocytotic elimination and domain-selective tethering constitute a potential mechanism of protein segregation at the axonal initial segment. J Cell Biol 166:571-578.
21. Frankenhaeuser B, Huxley AF (1964) The action potential in the myelinated nerve fiber of Xenopus laevis as computed on the basis of voltage clamp data. J Physiol (Lond) 171:302-315.
22. Fritschy JM, Weinmann O, Wenzel A, Benke D (1998) Synapse-specific localization of NMDA and GABA(A) receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194-210.
23. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B (2003) A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300:2091-2094.
24. Garver TD, Ren Q, Tuvia S, Bennett V (1997) Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J Cell Biol 137:703-714.
25. Gokin AP, Philip B, Strichartz GR (2001) Preferential block of small myelinated sensory and motor fibers by lidocaine: in vivo electrophysiology in the rat sciatic nerve. Anesthesiology 95:1441-1454.
26. + channels. J Exp Biol 205:575-584.
27. Gribkoff VK (2003) The therapeutic potential of neuronal KCNQ channel modulators. Expert Opin Ther Targets 7:737-748.
28. Hadley JK, Noda M, Selyanko AA, Wood IC, Abogadie FC, Brown DA (2000) Differential tetraethylammonium sensitivity of KCNQ1-4 potassium channels. Br J Pharmacol 129:413-415.
29. Hadley JK, Passmore GM, Tatulian L, Al-Qatari M, Ye F, Wickenden AD, Brown DA (2003) Stoichiometry of expressed KCNQ2/KCNQ3 potassium channels and subunit composition of native ganglionicMchannels deduced from block by tetraethylammonium. J Neurosci 23:5012-5019.
30. Herson PS, Virk M, Rustay NR, Bond CT, Crabbe JC, Adelman JP, Maylie J (2003) A mouse model of episodic ataxia type-1. Nat Neurosci 6:378-383.
31. Hille B (2001) Ionic channels of excitable membranes, Ed 3. Sunderland, MA: Sinauer.
32. Hoshi N, Zhang JS, Omaki M, Takeuchi T, Yokoyama S, Wanaverbecq N, Langeberg LK, Yoneda Y, Scott JD, Brown DA, Higashida H (2003) AKAP150 signaling complex promotes suppression of the M-current by muscarinic agonists. Nat Neurosci 6:564-571.
33. Howard A, Tamas G, Soltesz I (2005) Lighting the chandelier: new vistas for axo-axonic cells. Trends Neurosci 28:310-316.
34. Jan LY, Jan YN (1982) Peptidergic transmission in sympathetic ganglia of the frog. J Physiol (Lond) 327:219-246.
35. Jenkins SM, Bennett V (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155:739-746.
36. 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.
37. Kosaka T (1980) The axon initial segment as a synaptic site: ultrastructure and synaptology of the initial segment of the pyramidal cell in the rat hippocampus (CA3 region). J Neurocytol 9:861-882.
38. +-channel proteins. Nature 374:135-141.
39. Lemaillet G, Walker B, Lambert S (2003) Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278:27333-27339.
40. Lerche C, Scherer CR, Seebohm G, Derst C, Wei AD, Busch AE, Steinmeyer K (2000) Molecular cloning and functional expression of KCNQ5, a potassium channel subunit that may contribute to neuronal M-current diversity. J Biol Chem 275:22395-22400.
41. Lippincott-Schwartz J, Altan-Bonnet N, Patterson GH (2003) Photobleaching and photoactivation: following protein dynamics in living cells. Nat Cell Biol Suppl:S7-S14.
42. Lock LF, Gilbert DJ, Street VA, Migeon MB, Jenkins NA, Copeland NG, Tempel BL (1994) Voltage-gated potassium channel genes are clustered in paralogous regions of the mouse genome. Genomics 20:354-362.
43. Müller BM, Kistner U, Kindler S, Chung WJ, Kuhlendahl S, Fenster SD, Lau LF, Veh RW, Huganir RL, Gundelfinger ED, Garner CC (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17:255-265.
44. + channels. Neuron 37:449-461.
45. Palay SL, Sotelo C, Peters A, Orkand PM (1968) The axon hillock and the initial segment. J Cell Biol 38:193-201.
46. 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.
47. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D (2005) Conditional transgenic suppression of M channels in mouse brains reveals functions in neuronal excitability, resonance and behavior. Nat Neurosci 8:51-60.
48. Plummer NW, Meisler MH (1999) Evolution and diversity of mammalian sodium channel genes. Genomics 57:323-331.
49. Rasband MN, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, Shrager P (1998) Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18:36-47.
50. + channels altered by presence of beta-subunit. Nature 369:289-294.
51. Röper J, Schwarz JR (1989) Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. J Physiol (Lond) 416:93-110.
52. + channels in brain. J Neurosci 21:4609-4624.
53. Scherer SS, Arroyo EJ (2002) Recent progress on the molecular organization of myelinated axons. J Peripher Nerv Syst 7:1-12.
54. Scherer SS, Deschenes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL (1995) Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15:8281-8294.
55. Schmalbruch H (1986) Fiber composition of the rat sciatic nerve. Anat Rec 215:71-81.
56. Schroeder BC, Kubisch C, Stein V, Jentsch TJ (1998) Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K channels causes epilepsy. Nature 396:687-690.
57. + channels involved in epilepsy. J Biol Chem 275:13343-13348.
58. + channel assembly. EMBO Rep 4:76-81.
59. Schwarz JR, Reid G, Bostock H (1995) Action potentials and membrane currents in the human node of Ranvier. Pflugers Arch 430:283-292.
60. Scriven DR, Dan P, Moore ED (2000) Distribution of proteins implicated in excitation-contraction coupling in rat ventricular myocytes. Biophys J 79:2682-2691.
61. Selyanko AA, Hadley JK, Brown DA (2001) Properties of single M-type KCNQ2/KCNQ3 potassium channels expressed in mammalian cells. J Physiol (Lond) 534:15-24.
62. Selyanko AA, Delmas P, Hadley JK, Tatulian L, Wood IC, Mistry M, London B, Brown DA (2002) Dominant-negative subunits reveal potassium channel families that contribute to M-like potassium currents. J Neurosci 22:RC212(1-5).
63. 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.
64. + channels that underlie the neuronalMcurrent. J Neurosci 20:1710-1721.
65. Shen W, Hamilton SE, Nathanson NM, Surmeier DJ (2005) Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J Neurosci 25:7449-7458.
66. Singh NA, Charlier C, Stauffer D, DuPont BR, Leach RJ, Melis R, Ronen GM, Bjerre I, Quattlebaum T, Murphy JV, McHarg ML, Gagnon D, Rosales TO, Peiffer A, Anderson VE, Leppert M (1998) A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat Genet 18:25-29.
67. Singh NA, Westenskow P, Charlier C, Pappas C, Leslie J, Dillon J, Anderson VE, Sanguinetti MC, Leppert MF (2003) KCNQ2 and KCNQ3 potassium channel genes in benign familial neonatal convulsions: expansion of the functional and mutation spectrum. Brain 126:2726-2737.
68. Smart S, Lopantsev V, Zhang CL, Robbins C, Wand H, Chiu SY, Schwartzkroin PA, Messing A, Tempel B (1998) Deletion of the Kv1.1 potassium channel causes epilepsy in mice. Neuron 20:809-820.
69. Stuart G, Spruston N, Sakmann B, Hausser M (1997) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20:125-131.
70. Stuhmer W, Conti F, Suzuki H, Wang XD, Noda M, Yahagi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597-603.
71. Surti TS, Huang L, Jan YN, Jan LY, Cooper EC (2005) Identification by mass spectrometry and functional characterization of two phosphorylation sites of KCNQ2/KCNQ3 channels. Proc Natl Acad Sci USA 102:17828-17833.
72. Swedlow JR, Platani M (2002) Live cell imaging using wide-field microscopy and deconvolution. Cell Struct Funct 27:335-341.
73. Tanimura N, Nagafuku M, Liddicoat DR, Hamaoka T, Kosugi A (2003) Analysis of the mobility of signaling molecules in lymphocytes using fluorescence photobleaching techniques. Sci STKE 2003:p110.
74. Vleggeert-Lankamp CL, van den Berg RJ, Feirabend HK, Lakke EA, Malessy MJ, Thomeer RT (2004) Electrophysiology and morphometry of the Aalpha- and Abeta-fiber populations in the normal and regenerating rat sciatic nerve. Exp Neurol 187:337-349.
75. Vogel W, Schwarz JR (1995) Voltage-clamp studies in axons: macroscopic and single-channel currents. In: The axon (Waxman SG, Kocsis JD, Stys PK, eds), pp 257-280. New York: Oxford UP.
76. + channels in terminal and juxtaparanodal regions of neurons. Nature 365:75-79.
77. Wang H-S, 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.
78. Wei AD, Butler A, Salkoff L (2005) KCNQ-like potassium channels in Caenorhabditis elegans. Conserved properties and modulation. J Biol Chem 280:21337-21345.
79. Wen H, Levitan IB (2002) Calmodulin is an auxiliary subunit of KCNQ2/ KCNQ3 potassium channels. J Neurosci 22:7991-8001.
80. Wen H, Weiger TM, Ferguson TS, Shahidullah M, Scott SS, Levitan IB (2005) A DrosophiliaKCNQchannel essential for early embryonic development. J Neurosci 25:10147-10156.
81. Winckler B (2004) Scientiae forum/models and speculations pathways for axonal targeting of membrane proteins. Biol Cell 96:669-674.
82. Winckler B, Forscher P, Mellman I (1999) A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397:698-701.
83. Yang WP, Levesque PC, Little WA, Conder ML, Ramakrishnan P, Neubauer MG, Blanar MA (1998) Functional expression of two KvLQT1-related potassium channels responsible for an inherited idiopathic epilepsy. J Biol Chem 273:19419-19423.
84. Yasargil GM, Greeff NG, Luescher HR, Akert K, Sandri C (1982) The structural correlate of saltatory conduction along the Mauthner axon in the tench (Tinca tinca L.): identification of nodal equivalents at the axon collaterals. J Comp Neurol 212:417-424.
85. Yu FH, Catterall WA (2004) The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004:re15.
86. Yus-Najera E, Santana-Castro I, Villarroel A (2002) The identification and characterization of a noncontinuous calmodulin-binding site in noninactivating voltage-dependent KCNQ potassium channels. J Biol Chem 277:28545-28553.
87. Zakon HH (2002) Convergent evolution on the molecular level. Brain Behav Evol 59:250-261.
88. Zalc B, Colman DR (2000) Origins of vertebrate success. Science 288:271-272.
89. Zhang D, Kiyatkin A, Bolin JT, Low PS (2000) Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood 96:2925-2933.
90. Zhang H, Craciun LC, Mirshahi T, Rohacs T, Lopes CM, Jin T, Logothetis DE (2003) PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963-975.
91. Zhang J, Kumar S (1997) Detection of convergent and parallel evolution at the amino acid sequence level. Mol Biol Evol 14:527-536.
92. Zhang X, Bennett V (1998) Restriction of 480/270-kD ankyrin G to axon proximal segments requires multiple ankyrin G-specific domains. J Cell Biol 142:1571-1581.
93. Zhang X, Davis JQ, Carpenter S, Bennett V (1998) Structural requirements for association of neurofascin with ankyrin. J Biol Chem 273:30785-30794.
94. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V (1998) AnkyrinG 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.
95. Zhou L, Messing A, Chiu SY (1999) Determinants of excitability at transition zones in Kv1.1-deficient myelinated nerves. J Neurosci 19:5768-5781.