Axon initial segments: Diverse and dynamic neuronal compartments

Current Opinion in Neurobiology

Volumn 27, Issue , 2014, Pages 96-102

  Yoshimura, Takeshi ^a,b   Rasband, Matthew N ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AXON INITIAL SEGMENT PROTEIN; CELL PROTEIN; UNCLASSIFIED DRUG; ANKYRIN;

AXON INITIAL SEGMENT; AXON INITIATION SEGMENT ASSEMBLY; AXON INITIATION SEGMENT DIVERSITY; CELL ACTIVITY; CELL COMPOSITION; CELL FUNCTION; CELL POLARITY; CELL STRUCTURE; HUMAN; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN PROCESSING; REVIEW; ANIMAL; CYTOLOGY; CYTOSKELETON; METABOLISM; NERVE FIBER; NONLINEAR SYSTEM; PHYSIOLOGY;

ANIMALS; ANKYRINS; AXONS; CELL POLARITY; CYTOSKELETON; HUMANS; NEURONS; NONLINEAR DYNAMICS;

EID: 84897461161     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.03.004     Document Type: Review

References (61)

1. Rasband M.N. The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 2010, 11:552-562.
2. Grubb M.S., Burrone J. Building and maintaining the axon initial segment. Curr Opin Neurobiol 2010, 20:481-488.
3. Leterrier C., Dargent B. No Pasaran! Role of the axon initial segment in the regulation of protein transport and the maintenance of axonal identity. Semin Cell Dev Biol 2014, (in press).
4. Nakada C., Ritchie K., Oba Y., Nakamura M., Hotta Y., Iino R., Kasai R.S., Yamaguchi K., Fujiwara T., Kusumi A. Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat Cell Biol 2003, 5:626-632.
5. Winckler B., Forscher P., Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 1999, 397:698-701.
6. Watanabe K., Al-Bassam S., Miyazaki Y., Wandless T.J., Webster P., Arnold D.B. Networks of polarized actin filaments in the axon initial segment provide a mechanism for sorting axonal and dendritic proteins. Cell Rep 2012, 2:1546-1553.
7. Nakata T., Hirokawa N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 2003, 162:1045-1055.
8. Song A.H., Wang D., Chen G., Li Y., Luo J., Duan S., Poo M.M. A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009, 136:1148-1160.
9. Hedstrom K.L., Ogawa Y., Rasband M.N. AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 2008, 183:635-640.
10. Sobotzik J.M., Sie J.M., Politi C., Del Turco D., Bennett V., Deller T., Schultz C. AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc Natl Acad Sci U S A 2009, 106:17564-17569.
11. Iqbal Z., Vandeweyer G., van der Voet M., Waryah A.M., Zahoor M.Y., Besseling J.A., Roca L.T., Vulto-van Silfhout A.T., Nijhof B., Kramer J.M., et al. Homozygous and heterozygous disruptions of ANK3: at the crossroads of neurodevelopmental and psychiatric disorders. Hum Mol Genet 2013, 22:1960-1970.
12. Kole M.H., Stuart G.J. Signal processing in the axon initial segment. Neuron 2012, 73:235-247.
13. Bender K.J., Trussell L.O. The physiology of the axon initial segment. Annu Rev Neurosci 2012, 35:249-265.
14. Grubb M.S., Burrone J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 2010, 465:1070-1074.
15. Kuba H., Oichi Y., Ohmori H. Presynaptic activity regulates Na+ channel distribution at the axon initial segment. Nature 2010, 465:1075-1078.
16. Hu W., Tian C., Li T., Yang M., Hou H., Shu Y. Distinct contributions of Nav1.6 and Nav1.2 in action potential initiation and backpropagation. Nat Neurosci 2009, 12:996-1002.
17. Lorincz A., Nusser Z. Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 2008, 28:14329-14340.
18. Puthussery T., Venkataramani S., Gayet-Primo J., Smith R.G., Taylor W.R. Nav1.1 channels in axon initial segments of bipolar cells augment input to magnocellular visual pathways in the primate retina. J Neurosci 2013, 33:16045-16059.
19. Van Wart A., Trimmer J.S., Matthews G. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 2007, 500:339-352.
20. Ogiwara I., Miyamoto H., Morita N., Atapour N., Mazaki E., Inoue I., Takeuchi T., Itohara S., Yanagawa Y., Obata K., et al. Nav1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J Neurosci 2007, 27:5903-5914.
21. 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.
22. Han S., Tai C., Westenbroek R.E., Yu F.H., Cheah C.S., Potter G.B., Rubenstein J.L., Scheuer T., de la Iglesia H.O., Catterall W.A. Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature 2012, 489:385-390.
23. Ogawa Y., Rasband M.N. The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol 2008, 18:307-313.
24. Ogawa Y., Horresh I., Trimmer J.S., Bredt D.S., Peles E., Rasband M.N. Postsynaptic density-93 clusters Kv1 channels at axon initial segments independently of Caspr2. J Neurosci 2008, 28:5731-5739.
25. Ji W., Li T., Pan Y., Tao H., Ju K., Wen Z., Fu Y., An Z., Zhao Q., Wang T., et al. CNTNAP2 is significantly associated with schizophrenia and major depression in the Han Chinese population. Psychiatry Res 2013, 207:225-228.
26. Penagarikano O., Abrahams B.S., Herman E.I., Winden K.D., Gdalyahu A., Dong H., Sonnenblick L.I., Gruver R., Almajano J., Bragin A., et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 2011, 147:235-246.
27. Bender K.J., Uebele V.N., Renger J.J., Trussell L.O. Control of firing patterns through modulation of axon initial segment T-type calcium channels. J Physiol 2012, 590:109-118.
28. Buffington S.A., Rasband M.N. Na+ channel-dependent recruitment of Navβ4 to axon initial segments and nodes of Ranvier. J Neurosci 2013, 33:6191-6202.
29. Inan M., Blazquez-Llorca L., Merchan-Perez A., Anderson S.A., DeFelipe J., Yuste R. Dense and overlapping innervation of pyramidal neurons by chandelier cells. J Neurosci 2013, 33:1907-1914.
30. Szabadics J., Varga C., Molnar G., Olah S., Barzo P., Tamas G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 2006, 311:233-235.
31. Lewis D.A. The chandelier neuron in schizophrenia. Dev Neurobiol 2011, 71:118-127.
32. Taniguchi H., Lu J., Huang Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 2013, 339:70-74.
33. Barnes A.P., Polleux F. Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 2009, 32:347-381.
34. Craig A.M., Banker G. Neuronal polarity. Annu Rev Neurosci 1994, 17:267-310.
35. Galiano M.R., Jha S., Ho T.S., Zhang C., Ogawa Y., Chang K.J., Stankewich M.C., Mohler P.J., Rasband M.N. A distal axonal cytoskeleton forms an intra-axonal boundary that controls axon initial segment assembly. Cell 2012, 149:1125-1139.
36. Zhang X., Bennett V. Restriction of 480/270-kD ankyrin G to axon proximal segments requires multiple ankyrin G-specific domains. J Cell Biol 1998, 142:1571-1581.
37. Zhang C., Susuki K., Zollinger D.R., Dupree J.L., Rasband M.N. Membrane domain organization of myelinated axons requires betaII spectrin. J Cell Biol 2013, 203:437-443.
38. Ogawa Y., Schafer D.P., Horresh I., Bar V., Hales K., Yang Y., Susuki K., Peles E., Stankewich M.C., Rasband M.N. Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J Neurosci 2006, 26:5230-5239.
39. Xu K., Zhong G., Zhuang X. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 2013, 339:452-456.
40. Komada M., Soriano P. βIV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 2002, 156:337-348.
41. Kaphzan H., Buffington S.A., Jung J.I., Rasband M.N., Klann E. Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of angelman syndrome. J Neurosci 2011, 31:17637-17648.
42. Kaphzan H., Buffington S.A., Ramaraj A.B., Lingrel J.B., Rasband M.N., Santini E., Klann E. Genetic reduction of the alpha1 subunit of Na/K-ATPase corrects multiple hippocampal phenotypes in Angelman syndrome. Cell Rep 2013, 4:405-412.
43. Baalman K.L., Cotton R.J., Rasband S.N., Rasband M.N. Blast wave exposure impairs memory and decreases axon initial segment length. J Neurotrauma 2013, 30:741-751.
44. Hinman J.D., Rasband M.N., Carmichael S.T. Remodeling of the axon initial segment after focal cortical and white matter stroke. Stroke 2013, 44:182-189.
45. Evans M.D., Sammons R.P., Lebron S., Dumitrescu A.S., Watkins T.B., Uebele V.N., Renger J.J., Grubb M.S. Calcineurin signaling mediates activity-dependent relocation of the axon initial segment. J Neurosci 2013, 33:6950-6963.
46. Trunova S., Baek B., Giniger E. Cdk5 regulates the size of an axon initial segment-like compartment in mushroom body neurons of the Drosophila central brain. J Neurosci 2011, 31:10451-10462.
47. Ren Q., Bennett V. Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J Neurochem 1998, 70:1839-1849.
48. He M., Jenkins P., Bennett V. Cysteine 70 of ankyrin-G is S-palmitoylated and is required for function of ankyrin-G in membrane domain assembly. J Biol Chem 2012, 287:43995-44005.
49. Bréchet A., Fache M.P., Brachet A., Ferracci G., Baude A., Irondelle M., Pereira S., Leterrier C., Dargent B. Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interactions with ankyrin G. J Cell Biol 2008, 183:1101-1114.
50. Sánchez-Ponce D., Muñoz A., Garrido J.J. Casein kinase 2 and microtubules control axon initial segment formation. Mol Cell Neurosci 2011, 46:222-234.
51. Hund T.J., Koval O.M., Li J., Wright P.J., Qian L., Snyder J.S., Gudmundsson H., Kline C.F., Davidson N.P., Cardona N., et al. A βIV-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest 2010, 120:3508-3519.
52. Vacher H., Yang J.W., Cerda O., Autillo-Touati A., Dargent B., Trimmer J.S. Cdk-mediated phosphorylation of the Kvβ2 auxiliary subunit regulates Kv1 channel axonal targeting. J Cell Biol 2011, 192:813-824.
53. Garver T.D., Ren Q., Tuvia S., Bennett V. 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 1997, 137:703-714.
54. Buffington S.A., Sobotzik J.M., Schultz C., Rasband M.N. IκBα is not required for axon initial segment assembly. Mol Cell Neurosci 2012, 50:1-9.
55. Tapia M., Del Puerto A., Puime A., Sanchez-Ponce D., Fronzaroli-Molinieres L., Pallas-Bazarra N., Carlier E., Giraud P., Debanne D., Wandosell F., et al. GSK3 and β-catenin determines functional expression of sodium channels at the axon initial segment. Cell Mol Life Sci 2013, 70:105-120.
56. Shavkunov A.S., Wildburger N.C., Nenov M.N., James T.F., Buzhdygan T.P., Panova-Elektronova N.I., Green T.A., Veselenak R.L., Bourne N., Laezza F. The fibroblast growth factor 14 voltage-gated sodium channel complex is a new target of glycogen synthase kinase 3 (GSK3). J Biol Chem 2013, 288:19370-19385.
57. Chen S., Owens G.C., Makarenkova H., Edelman D.B. HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS ONE 2010, 5:e10848.
58. Tapia M., Wandosell F., Garrido J.J. Impaired function of HDAC6 slows down axonal growth and interferes with axon initial segment development. PLoS ONE 2010, 5:e12908.
59. Leterrier C., Vacher H., Fache M.P., d'Ortoli S.A., Castets F., Autillo-Touati A., Dargent B. End-binding proteins EB3 and EB1 link microtubules to ankyrin G in the axon initial segment. Proc Natl Acad Sci U S A 2011, 108:8826-8831.
60. Yoshimura T., Kawano Y., Arimura N., Kawabata S., Kikuchi A., Kaibuchi K. GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005, 120:137-149.
61. Maniar T.A., Kaplan M., Wang G.J., Shen K., Wei L., Shaw J.E., Koushika S.P., Bargmann C.I. UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat Neurosci 2012, 15:48-56.