Preferential targeting of Nav1.6 voltage-gated Na+ channels to the axon initial segment during development

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Akin, Elizabeth J ^a   Solé, Laura ^a   Dib Hajj, Sulayman D ^b,c   Waxman, Stephen G ^b,c   Tamkun, Michael M ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRING; POTASSIUM CHANNEL KV2.1; SHAB POTASSIUM CHANNEL; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.6; UNCLASSIFIED DRUG; ANK3 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN BINDING; SCN8A PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AXON INITIAL SEGMENT; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; EMBRYO; HIPPOCAMPAL NEURONAL CULTURE; NERVE FIBER; NERVE FIBER MEMBRANE; NERVE GROWTH; NONHUMAN; ACTION POTENTIAL; ANIMAL; AXON; CYTOLOGY; EMBRYOLOGY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION REGULATION; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HIPPOCAMPUS; MAMMALIAN EMBRYO; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PRIMARY CELL CULTURE; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TRANSPORT VESICLE; TUMOR CELL LINE; ULTRASTRUCTURE;

ACTION POTENTIALS; ANIMALS; ANKYRINS; AXONS; CELL LINE, TUMOR; EMBRYO, MAMMALIAN; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MICE; NAV1.6 VOLTAGE-GATED SODIUM CHANNEL; NEUROGENESIS; PRIMARY CELL CULTURE; PROTEIN BINDING; RATS; RECOMBINANT FUSION PROTEINS; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSPORT VESICLES;

EID: 84929500906     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124397     Document Type: Article

References (36)

1. Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action Potential Generation Requires a High Sodium Channel Density in the Axon Initial Segment. Nat Neurosci. 2008 Feb; 11 (2):178-86. PMID: 18204443. doi: 10.1038/nn2040
2. Isom LL, De Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, et al. Primary Structure and Functional Expression of the Beta 1 Subunit of the Rat Brain Sodium Channel. Science. 1992 May 8; 256(5058):839-42. PMID: 1375395.
3. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. Xlvii. Nomenclature and Structure-Function Relationships of Voltage-Gated Sodium Channels. Pharmacol Rev. 2005 Dec; 57 (4):397-409. PMID: 16382098
4. Hu W, Tian C, Li T, Yang M, Hou H, Shu Y. Distinct Contributions of Na(V)1.6 and Na(V)1.2 in Action Potential Initiation and Backpropagation. Nat Neurosci. 2009 Aug; 12(8):996-1002. PMID: 19633666. doi: 10.1038/nn.2359
5. Lorincz A, Nusser Z. Cell-Type-Dependent Molecular Composition of the Axon Initial Segment. J Neurosci. 2008 Dec 31; 28(53):14329-40. PMID: 19118165. Pubmed Central PMCID: 2628579. doi: 10.1523/JNEUROSCI.4833-08.2008
6. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, Matthews G. Functional Specialization of the Axon Initial Segment by Isoform-Specific Sodium Channel Targeting. J Neurosci. 2003 Mar 15; 23(6):2306-13. PMID: 12657689.
7. Ogawa Y, Rasband MN. The Functional Organization and Assembly of the Axon Initial Segment. Current Opinion Neurobiol. 2008 Jun; 18(3):307-13. PMID: 18801432. doi: 10.1016/j.conb.2008.08.008
8. Dotti CG, Sullivan CA, Banker GA. The Establishment of Polarity by Hippocampal Neurons in Culture. J Neurosci. 1988 Apr; 8(4):1454-68. PMID: 3282038.
9. Hedstrom KL, Ogawa Y, Rasband MN. Ankyring Is Required for Maintenance of the Axon Initial Segment and Neuronal Polarity. J Cell Biol. 2008 Nov 17; 183(4):635-40. PMID: 19001126. Pubmed Central PMCID: 2582894. doi: 10.1083/jcb.200806112
10. Galiano MR, Jha S, Ho TS, Zhang C, Ogawa Y, Chang KJ, et al. A Distal Axonal Cytoskeleton Forms an Intra-Axonal Boundary That Controls Axon Initial Segment Assembly. Cell. 2012 May 25; 149 (5):1125-39. PMID: 22632975. Pubmed Central PMCID: 3361702. doi: 10.1016/j.cell.2012.03.039
11. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, et al. A Targeting Motif Involved in Sodium Channel Clustering at the Axonal Initial Segment. Science. 2003 Jun 27; 300(5628):2091-4. PMID: 12829783.
12. Lemaillet G, Walker B, Lambert S. Identification of a Conserved Ankyrin-Binding Motif in the Family of Sodium Channel Alpha Subunits. J Biol Chem. 2003 Jul 25; 278(30):27333-9. PMID: 12716895.
13. Gasser A, Ho TS, Cheng X, Chang KJ, Waxman SG, Rasband MN, et al. An Ankyring-Binding Motif Is Necessary and Sufficient for Targeting Nav1.6 Sodium Channels to Axon Initial Segments and Nodes of Ranvier. J Neurosci. 2012 May 23; 32(21):7232-43. PMID: 22623668. Pubmed Central PMCID: 3413458. doi: 10.1523/JNEUROSCI.5434-11.2012
14. Brechet A, Fache MP, Brachet A, Ferracci G, Baude A, Irondelle M, et al. Protein Kinase Ck2 Contributes to the Organization of Sodium Channels in Axonal Membranes by Regulating Their Interactions with Ankyrin G. J Cell Biol. 2008 Dec 15; 183(6):1101-14. PMID: 19064667. Pubmed Central PMCID: 2600743. doi: 10.1083/jcb.200805169
15. Garrido JJ, Fernandes F, Giraud P, Mouret I, Pasqualini E, Fache MP, et al. Identification of an Axonal Determinant in the C-Terminus of the Sodium Channel Na(V)1.2. EMBO J. 2001 Nov 1; 20(21):5950-61. PMID: 11689435
16. Fache MP, Moussif A, Fernandes F, Giraud P, Garrido JJ, Dargent B. Endocytotic Elimination and Domain-Selective Tethering Constitute a Potential Mechanism of Protein Segregation at the Axonal Initial Segment. J Cell Biol. 2004 Aug 16; 166(4):571-8. PMID: 15302857. Pubmed Central PMCID: 2172218.
17. Lee A, Goldin AL. Role of the Terminal Domains in Sodium Channel Localization. Channels (Austin). 009 May-Jun; 3(3):171-80. Epub 2009 May 24. PMID: 19535906
18. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, Waxman SG. Distinct Repriming and Closed-State Inactivation Kinetics of Nav1.6 and Nav1.7 Sodium Channels in Mouse Spinal Sensory Neurons. J Physiol. 2003 Sep 15; 551(Pt 3):741-50. PMID: 12843211. Pubmed Central PMCID: 2343279.
19. O'Connell KM, Rolig AS, Whitesell JD, Tamkun MM. Kv2.1 Potassium Channels Are Retained within Dynamic Cell Surface Microdomains That Are Defined by a Perimeter Fence. J Neurosci. 2006 Sep 20; 26(38):9609-18. PMID: 16988031.
20. Brachet A, Leterrier C, Irondelle M, Fache MP, Racine V, Sibarita JB, et al. Ankyrin G Restricts Ion Channel Diffusion at the Axonal Initial Segment before the Establishment of the Diffusion Barrier. J Cell Biol. 2010 Oct 18; 191(2):383-95. PMID: 20956383. Pubmed Central PMCID: 2958486. doi: 10.1083/jcb.201003042
21. Tamkun MM, O'Connell K M, Rolig AS. A Cytoskeletal-Based Perimeter Fence Selectively Corrals a Sub-Population of Cell Surface Kv2.1 Channels. J Cell Sci. 2007 Jul 15; 120(Pt 14):2413-23. PMID: 17606996.
22. Deutsch E, Weigel AV, Akin EJ, Fox P, Hansen G, Haberkorn CJ, et al. Kv2.1 Cell Surface Clusters Are Insertion Platforms for Ion Channel Delivery to the Plasma Membrane. Molecular biology of the cell. 2012 Aug; 23(15):2917-29. PMID: 22648171. Pubmed Central PMCID: 3408418. doi: 10.1091/mbc.E12-01-0047
23. Zhang JZ, Yarov-Yarovoy V, Scheuer T, Karbat I, Cohen L, Gordon D, et al. Mapping the Interaction Site for a Beta-Scorpion Toxin in the Pore Module of Domain Iii of Voltage-Gated Na(+) Channels. J Biol Chem. 2012 Aug 31; 287(36):30719-28. PMID: 22761417. Pubmed Central PMCID: 3436316. doi: 10.1074/jbc.M112.370742
24. Chen I, Howarth M, Lin W, Ting AY. Site-Specific Labeling of Cell Surface Proteins with Biophysical Probes Using Biotin Ligase. Nat Methods. 2005 Feb; 2(2):99-104. PMID: 15782206.
25. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR. Sodium Channel Na(V)1.6 Is Localized at Nodes of Ranvier, Dendrites, and Synapses. Proc Natl Acad Sci U S A. 2000 May 9; 97(10):5616-20. PMID: 10779552. Pubmed Central PMCID: 25877.
26. Jenkins SM, Bennett V. 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. 2001 Nov 26; 155(5):739-46. PMID: 11724816. Pubmed Central PMCID: 2150881.
27. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG. Sodium Channel Alpha-Subunit Mrnas I, Ii, Iii, Nag, Na6 and Hne (Pn1): Different Expression Patterns in Developing Rat Nervous System. Brain Res Mol Brain Res 1997 Apr; 45(1):71-82. PMID: 9105672.
28. Gasser A, Cheng X, Gilmore ES, Tyrrell L, Waxman SG, Dib-Hajj SD. Two Nedd4-Binding Motifs Underlie Modulation of Sodium Channel Nav1.6 by P38 Mapk. J Biol Chem. 2010 Aug 20; 285 (34):26149-61. doi: 10.1074/jbc.M109.098681 Epub 2010 Jun 8. PMID: 20530479
29. Smith MR, Smith RD, Plummer NW, Meisler MH, Goldin AL. Functional Analysis of the Mouse Scn8a Sodium Channel. J Neurosci. 1998 Aug 15; 18(16):6093-102. PMID: 9698304.
30. Nakada C, Ritchie K, Oba Y, Nakamura M, Hotta Y, Iino R, et al. Accumulation of Anchored Proteins Forms Membrane Diffusion Barriers During Neuronal Polarization. Nat Cell Biol. 2003 Jul; 5(7):626-32. PMID: 12819789.
31. Xu K, Zhong G, Zhuang X. Actin, Spectrin, and Associated Proteins Form a Periodic Cytoskeletal Structure in Axons. Science. 2013 Feb 25; 339(6118):452-6. PMID: 23239625. doi: 10.1126/science.1232251
32. Barry J, Gu Y, Jukkola P, O'Neill B, Gu H, Mohler PJ, et al. Ankyrin-G Directly Binds to Kinesin-1 to Transport Voltage-Gated Na+ Channels into Axons. Dev Cell. 2014 Jan 27; 28(2):117-31. doi: 10.1016/j.devcel.2013.11.023 PMID: 24412576
33. Leterrier C, Dargent B. No Pasaran! Role of the Axon Initial Segment in the Regulation of Protein Transport and the Maintenance of Axonal Identity. Sem Cell Devel Biol. 2014 Mar; 27C:44-51. PMID: 24239676.
34. Malhotra JD, Koopmann MC, Kazen-Gillespie KA, Fettman N, Hortsch M, Isom LL. Structural Requirements for Interaction of Sodium Channel Beta 1 Subunits with Ankyrin. J Biol Chem. 2002 Jul 19; 277(29):26681-8. PMID: 11997395.
35. Brackenbury WJ, Calhoun JD, Chen C, Miyazaki H, Nukina N, Oyama F, et al. Functional Reciprocity between Na+ Channel Nav1.6 and Beta1 Subunits in the Coordinated Regulation of Excitability and Neurite Outgrowth. Proc Natl Acad Sci U S A. 2010 Feb 2; 107(5):2283-8. PMID: 20133873. Pubmed Central PMCID: PMC2836661. doi: 10.1073/pnas.0909434107
36. Jones SL, Korobova F, Svitkina T. Axon Initial Segment Cytoskeleton Comprises a Multiprotein Submembranous Coat Containing Sparse Actin Filaments. J Cell Biol. 2014 Apr 14; 205(1):67-81. PMID: 24711503. Pubmed Central PMCID: 3987141. doi: 10.1083/jcb.201401045