Characterization of the axon initial segment (AIS) of motor neurons and identification of a para-AIS and a juxtapara-AIS, organized by protein 4.1B

BMC Biology

Volumn 9, Issue , 2011, Pages

  Duflocq, Amandine ^a,b,c   Chareyre, Fabrice ^d   Giovannini, Marco ^d   Couraud, François ^a,b,c   Davenne, Marc ^a,b,c  

^a INSERM   (France)

^b Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d HOUSE RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUS;

ACTIN BINDING PROTEIN; AXONIN 1; CNTNAP2 PROTEIN, MOUSE; DLGH2 PROTEIN, MOUSE; EPB4.1L3 PROTEIN, MOUSE; GUANYLATE KINASE; MEMBRANE PROTEIN; NERVE PROTEIN; SODIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CLUSTER ANALYSIS; METABOLISM; MOTONEURON; MOUSE; NERVE FIBER;

ANIMALS; AXONS; CLUSTER ANALYSIS; CONTACTIN 2; GUANYLATE KINASE; MEMBRANE PROTEINS; MICE; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MOTOR NEURONS; NERVE TISSUE PROTEINS; POTASSIUM CHANNELS, VOLTAGE-GATED; SODIUM CHANNELS;

EID: 80054894583     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-9-66     Document Type: Article

References (62)

1. Bean BP. The action potential in mammalian central neurons. Nat Rev Neurosci 2007, 8:451-465.
2. Kuba H, Ishii TM, Ohmori H. Axonal site of spike initiation enhances auditory coincidence detection. Nature 2006, 444:1069-1072. 10.1038/nature05347, 17136099.
3. Grubb MS, Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 2010, 465:1070-1074. 10.1038/nature09160, 20543823.
4. Kuba H, Oichi Y, Ohmori H. Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 2010, 465:1075-1078. 10.1038/nature09087, 20543825.
5. 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, 23:2306-2313.
6. 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, 155:739-746. 10.1083/jcb.200109026, 2150881, 11724816.
7. Van Wart A, Trimmer JS, Matthews G. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 2007, 500:339-352. 10.1002/cne.21173, 17111377.
8. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B. A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 2003, 300:2091-2094. 10.1126/science.1085167, 12829783.
9. 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, 278:27333-27339. 10.1074/jbc.M303327200, 12716895.
10. Kordeli E, Lambert S, Bennett V. AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 1995, 270:2352-2359. 10.1074/jbc.270.5.2352, 7836469.
11. Inda MC, DeFelipe J, Munoz A. Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci USA 2006, 103:2920-2925. 10.1073/pnas.0511197103, 1413846, 16473933.
12. Kole MH, Letzkus JJ, Stuart GJ. Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 2007, 55:633-647. 10.1016/j.neuron.2007.07.031, 17698015.
13. Lorincz A, Nusser Z. Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 2008, 28:14329-14340. 10.1523/JNEUROSCI.4833-08.2008, 2628579, 19118165.
14. Goldberg EM, Clark BD, Zagha E, Nahmani M, Erisir A, Rudy B. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 2008, 58:387-400. 10.1016/j.neuron.2008.03.003, 2730466, 18466749.
15. Ogawa Y, Horresh I, Trimmer JS, Bredt DS, Peles E, Rasband MN. Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2. J Neurosci 2008, 28:5731-5739. 10.1523/JNEUROSCI.4431-07.2008, 2729199, 18509034.
16. Devaux JJ, Kleopa KA, Cooper EC, Scherer SS. KCNQ2 is a nodal K+ channel. J Neurosci 2004, 24:1236-1244. 10.1523/JNEUROSCI.4512-03.2004, 14762142.
17. Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, Bennett V, Scherer SS, Cooper EC. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 2006, 26:2599-2613. 10.1523/JNEUROSCI.4314-05.2006, 16525039.
18. Chung HJ, Jan YN, Jan LY. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc Natl Acad Sci USA 2006, 103:8870-8875. 10.1073/pnas.0603376103, 1472242, 16735477.
19. Ogawa Y, Oses-Prieto J, Kim MY, Horresh I, Peles E, Burlingame AL, Trimmer JS, Meijer D, Rasband MN. ADAM22, a Kv1 channel-interacting protein, recruits membrane-associated guanylate kinases to juxtaparanodes of myelinated axons. J Neurosci 2010, 30:1038-1048. 10.1523/JNEUROSCI.4661-09.2010, 2811262, 20089912.
20. Traka M, Goutebroze L, Denisenko N, Bessa M, Nifli A, Havaki S, Iwakura Y, Fukamauchi F, Watanabe K, Soliven B, Girault JA, Karagogeos D. Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J Cell Biol 2003, 162:1161-1172. 10.1083/jcb.200305078, 2172849, 12975355.
21. Poliak S, Salomon D, Elhanany H, Sabanay H, Kiernan B, Pevny L, Stewart CL, Xu X, Chiu SY, Shrager P, Furley AJ, Peles E. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1. J Cell Biol 2003, 162:1149-1160. 10.1083/jcb.200305018, 2172860, 12963709.
22. Savvaki M, Panagiotaropoulos T, Stamatakis A, Sargiannidou I, Karatzioula P, Watanabe K, Stylianopoulou F, Karagogeos D, Kleopa KA. Impairment of learning and memory in TAG-1 deficient mice associated with shorter CNS internodes and disrupted juxtaparanodes. Mol Cell Neurosci 2008, 39:478-490. 10.1016/j.mcn.2008.07.025, 18760366.
23. Savvaki M, Theodorakis K, Zoupi L, Stamatakis A, Tivodar S, Kyriacou K, Stylianopoulou F, Karagogeos D. The expression of TAG-1 in glial cells is sufficient for the formation of the juxtaparanodal complex and the phenotypic rescue of tag-1 homozygous mutants in the CNS. J Neurosci 2010, 30:13943-13954. 10.1523/JNEUROSCI.2574-10.2010, 20962216.
24. Dupree JL, Girault JA, Popko B. Axo-glial interactions regulate the localization of axonal paranodal proteins. J Cell Biol 1999, 147:1145-1152. 10.1083/jcb.147.6.1145, 2168103, 10601330.
25. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 2001, 30:369-383. 10.1016/S0896-6273(01)00294-X, 11395000.
26. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 2001, 30:385-397. 10.1016/S0896-6273(01)00296-3, 11395001.
27. Poliak S, Gollan L, Salomon D, Berglund EO, Ohara R, Ranscht B, Peles E. Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J Neurosci 2001, 21:7568-7575.
28. Denisenko-Nehrbass N, Oguievetskaia K, Goutebroze L, Galvez T, Yamakawa H, Ohara O, Carnaud M, Girault JA. Protein 4.1B associates with both Caspr/paranodin and Caspr2 at paranodes and juxtaparanodes of myelinated fibres. Eur J Neurosci 2003, 17:411-416. 10.1046/j.1460-9568.2003.02441.x, 12542678.
29. Horresh I, Bar V, Kissil JL, Peles E. Organization of myelinated axons by Caspr and Caspr2 requires the cytoskeletal adapter protein 4.1B. J Neurosci 2010, 30:2480-2489. 10.1523/JNEUROSCI.5225-09.2010, 2836844, 20164332.
30. Burke R. Spinal cord: Ventral horn. The Synaptic Organization of the Brain 2004, 79-123. New York, USA: Oxford University Press, Shepherd GM.
31. Duflocq A, Le Bras B, Bullier E, Couraud F, Davenne M. Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci 2008, 39:180-192. 10.1016/j.mcn.2008.06.008, 18621130.
32. Greene LA. A new neuronal intermediate filament protein. Trends Neurosci 1989, 12:228-230. 10.1016/0166-2236(89)90127-6, 2473559.
33. Houser CR, Crawford GD, Barber RP, Salvaterra PM, Vaughn JE. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 1983, 266:97-119. 10.1016/0006-8993(83)91312-4, 6850348.
34. Rasband MN. The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 2010, 11:552-562. 10.1038/nrn2852, 20631711.
35. Friese A, Kaltschmidt JA, Ladle DR, Sigrist M, Jessell TM, Arber S. Gamma and alpha motor neurons distinguished by expression of transcription factor Err3. Proc Natl Acad Sci USA 2009, 106:13588-13593. 10.1073/pnas.0906809106, 2716387, 19651609.
36. Rhodes KJ, Strassle BW, Monaghan MM, Bekele-Arcuri Z, Matos MF, Trimmer JS. Association and colocalization of the Kvbeta1 and Kvbeta2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes. J Neurosci 1997, 17:8246-8258.
37. Vabnick I, Trimmer JS, Schwarz TL, Levinson SR, Risal D, Shrager P. Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J Neurosci 1999, 19:747-758.
38. Fukamauchi F, Aihara O, Wang YJ, Akasaka K, Takeda Y, Horie M, Kawano H, Sudo K, Asano M, Watanabe K, Iwakura Y. TAG-1-deficient mice have marked elevation of adenosine A1 receptors in the hippocampus. Biochem Biophys Res Commun 2001, 281:220-226. 10.1006/bbrc.2001.4334, 11178983.
39. Horresh I, Poliak S, Grant S, Bredt D, Rasband MN, Peles E. Multiple molecular interactions determine the clustering of Caspr2 and Kv1 channels in myelinated axons. J Neurosci 2008, 28:14213-14222. 10.1523/JNEUROSCI.3398-08.2008, 2859216, 19109503.
40. McGee AW, Topinka JR, Hashimoto K, Petralia RS, Kakizawa S, Kauer FW, Aguilera-Moreno A, Wenthold RJ, Kano M, Bredt DS. PSD-93 knock-out mice reveal that neuronal MAGUKs are not required for development or function of parallel fiber synapses in cerebellum. J Neurosci 2001, 21:3085-3091.
41. Baines AJ. The spectrin-ankyrin-4.1-adducin membrane skeleton: adapting eukaryotic cells to the demands of animal life. Protoplasma 2010, 244:99-131. 10.1007/s00709-010-0181-1, 20668894.
42. Gollan L, Sabanay H, Poliak S, Berglund EO, Ranscht B, Peles E. Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J Cell Biol 2002, 157:1247-1256. 10.1083/jcb.200203050, 2173544, 12082082.
43. Conradi S, Skoglund S. Observations on the ultrastructure of the initial motor axon segment and dorsal root boutons on the motoneurons in the lumbosacral spinal cord of the cat during postnatal development. Acta Physiol Scand Suppl 1969, 333:53-76.
44. Hausser M, Stuart G, Racca C, Sakmann B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 1995, 15:637-647. 10.1016/0896-6273(95)90152-3, 7546743.
45. Morgan CW. Axons of sacral preganglionic neurons in the cat: I. Origin, initial segment, and myelination. J Neurocytol 2001, 30:523-544. 10.1023/A:1015649419346, 12037468.
46. Lee DC, Jensen AL, Schiefer MA, Morgan CW, Grill WM. Structural mechanisms to produce differential dendritic gains. Brain Res 2005, 1033:117-127. 10.1016/j.brainres.2004.11.034, 15694915.
47. 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, 12:996-1002. 10.1038/nn.2359, 19633666.
48. Rush AM, Dib-Hajj SD, Waxman SG. Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones. J Physiol 2005, 564:803-815. 10.1113/jphysiol.2005.083089, 1464456, 15760941.
49. Kernell D. The Motoneuron and its Muscle Fibers 2006, Oxford, UK: Oxford University Press.
50. Manuel M, Iglesias C, Donnet M, Leroy F, Heckman CJ, Zytnicki D. Fast kinetics, high-frequency oscillations, and subprimary firing range in adult mouse spinal motoneurons. J Neurosci 2009, 29:11246-11256.
51. Meehan CF, Sukiasyan N, Zhang M, Nielsen JB, Hultborn H. Intrinsic properties of mouse lumbar motoneurons revealed by intracellular recording in vivo. J Neurophysiol 2010, 103:2599-2610. 10.1152/jn.00668.2009, 20164401.
52. Brown DA, Passmore GM. Neural KCNQ (Kv7) channels. Br J Pharmacol 2009, 156:1185-1195. 10.1111/j.1476-5381.2009.00111.x, 2697739, 19298256.
53. Shah MM, Migliore M, Valencia I, Cooper EC, Brown DA. Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 2008, 105:7869-7874. 10.1073/pnas.0802805105, 2408483, 18515424.
54. Li YC, Cheng CX, Li YN, Shimada O, Atsumi S. Beyond the initial axon segment of the spinal motor axon: fasciculated microtubules and polyribosomal clusters. J Anat 2005, 206:535-542. 10.1111/j.1469-7580.2005.00418.x, 1571525, 15960764.
55. Patino GA, Isom LL. Electrophysiology and beyond: multiple roles of Na+ channel beta subunits in development and disease. Neurosci Lett 2010, 486:53-59. 10.1016/j.neulet.2010.06.050, 20600605.
56. Rasband MN. Clustered K+ channel complexes in axons. Neurosci Lett 2010, 486:101-106. 10.1016/j.neulet.2010.08.081, 20816921.
57. Karnak D, Lee S, Margolis B. Identification of multiple binding partners for the amino-terminal domain of synapse-associated protein 97. J Biol Chem 2002, 277:46730-46735. 10.1074/jbc.M208781200, 12351654.
58. Shingai T, Ikeda W, Kakunaga S, Morimoto K, Takekuni K, Itoh S, Satoh K, Takeuchi M, Imai T, Monden M, Takai Y. Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAM1 in cell-cell adhesion and transmembrane protein localization in epithelial cells. J Biol Chem 2003, 278:35421-35427. 10.1074/jbc.M305387200, 12826663.
59. Yageta M, Kuramochi M, Masuda M, Fukami T, Fukuhara H, Maruyama T, Shibuya M, Murakami Y. Direct association of TSLC1 and DAL-1, two distinct tumor suppressor proteins in lung cancer. Cancer Res 2002, 62:5129-5133.
60. Gao B-X, Ziskind-Conhaim L. Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 1998, 80:3047-3061.
61. Buttermore ED, Dupree JL, Cheng JG, An X, Tessarollo L, Bhat MA. The cytoskeletal adaptor protein band 4.1B is required for the maintenance of paranodal axoglial septate junctions in myelinated axons. J Neurosci 2011, 31:8013-8024. 10.1523/JNEUROSCI.1015-11.2011, 21632923.
62. Cifuentes-Diaz C, Chareyre F, Garcia M, Devaux J, Carnaud M, Levasseur G, Niwa-Kawakita M, Harroch S, Girault J-A, Giovannini M, Goutebroze L. Protein 4.1B contributes to the organization of peripheral myelinated axons. PLoS ONE 2011, 6:e25043.