Nanoscale Architecture of the Axon Initial Segment Reveals an Organized and Robust Scaffold

Cell Reports

Volumn 13, Issue 12, 2015, Pages 2781-2793

  Leterrier, Christophe ^a   Potier, Jean ^a   Caillol, Ghislaine ^a   Debarnot, Claire ^a   Rueda Boroni, Fanny ^a   Dargent, Bénédicte ^a  

^a University of Mediterranée   (France)

Author keywords

ankyrin G; axon initial segment; cytoskeleton; scaffold; super resolution microscopy

Indexed keywords

ALPHA TUBULIN; ANKYRIN; EPITOPE; MOLECULAR SCAFFOLD; NOCODAZOLE; SPECTRIN;

AMINO TERMINAL SEQUENCE; ARTICLE; AXON INITIAL SEGMENT; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOARCHITECTURE; CYTOSKELETON; CYTOSOL; DEPOLYMERIZATION; LABELING INDEX; MEMBRANE STABILIZATION; MICROSCOPY; MICROTUBULE ASSEMBLY; NANOANALYSIS; NANOTECHNOLOGY; PERIODICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; QUANTITATIVE ANALYSIS; STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; THREE DIMENSIONAL IMAGING; ANIMAL; AXON; NERVE CELL; PHYSIOLOGY; RAT; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; ANKYRINS; AXONS; CYTOSKELETON; NEURONS; RATS; RATS, WISTAR;

EID: 84959410502     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.051     Document Type: Article

References (42)

1. Bennett, V., Lorenzo, D.N., Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Curr. Top. Membr. 72 (2013), 1–37.
2. Bennett, V., Davis, J., Fowler, W.E., Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin. Nature 299 (1982), 126–131.
3. 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. 183 (2008), 1101–1114.
4. D'Este, E., Kamin, D., Göttfert, F., El-Hady, A., Hell, S.W., STED nanoscopy reveals the ubiquity of subcortical cytoskeleton periodicity in living neurons. Cell Rep. 10 (2015), 1246–1251.
5. Davis, J.Q., Lambert, S., Bennett, V., Molecular composition of the node of Ranvier: identification of ankyrin-binding cell adhesion molecules neurofascin (mucin+/third FNIII domain-) and NrCAM at nodal axon segments. J. Cell Biol. 135 (1996), 1355–1367.
6. Grubb, M.S., Burrone, J., Building and maintaining the axon initial segment. Curr. Opin. Neurobiol. 20 (2010), 481–488.
7. Grubb, M.S., Burrone, J., Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465 (2010), 1070–1074.
8. Hedstrom, K.L., Xu, X., Ogawa, Y., Frischknecht, R., Seidenbecher, C.I., Shrager, P., Rasband, M.N., Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J. Cell Biol. 178 (2007), 875–886.
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. 183 (2008), 635–640.
10. 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. 22 (2013), 1960–1970.
11. Iwakura, A., Uchigashima, M., Miyazaki, T., Yamasaki, M., Watanabe, M., Lack of molecular-anatomical evidence for GABAergic influence on axon initial segment of cerebellar Purkinje cells by the pinceau formation. J. Neurosci. 32 (2012), 9438–9448.
12. Jaworski, J., Kapitein, L.C., Gouveia, S.M., Dortland, B.R., Wulf, P.S., Grigoriev, I., Camera, P., Spangler, S.A., Di Stefano, P., Demmers, J., et al. Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61 (2009), 85–100.
13. Jenkins, S.M., 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. 155 (2001), 739–746.
14. Jenkins, P.M., Kim, N., Jones, S.L., Tseng, W.-C., Svitkina, T.M., Yin, H.H., Bennett, V., Giant ankyrin-G: a critical innovation in vertebrate evolution of fast and integrated neuronal signaling. Proc. Natl. Acad. Sci. USA 112 (2015), 957–964.
15. Jones, S.L., Korobova, F., Svitkina, T., Axon initial segment cytoskeleton comprises a multiprotein submembranous coat containing sparse actin filaments. J. Cell Biol. 205 (2014), 67–81.
16. Kaech, S., Banker, G., Culturing hippocampal neurons. Nat. Protoc. 1 (2006), 2406–2415.
17. Kapitein, L.C., Hoogenraad, C.C., Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol. Cell. Neurosci. 46 (2011), 9–20.
18. Lacas-Gervais, S., Guo, J., Strenzke, N., Scarfone, E., Kolpe, M., Jahkel, M., De Camilli, P., Moser, T., Rasband, M.N., Solimena, M., BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J. Cell Biol. 166 (2004), 983–990.
19. Le Bras, B., Fréal, A., Czarnecki, A., Legendre, P., Bullier, E., Komada, M., Brophy, P.J., Davenne, M., Couraud, F., In vivo assembly of the axon initial segment in motor neurons. Brain Struct. Funct. 219 (2013), 1433–1450.
20. 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. 27 (2014), 44–51.
21. 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. USA 108 (2011), 8826–8831.
22. Leussis, M.P., Madison, J.M., Petryshen, T.L., Ankyrin 3: genetic association with bipolar disorder and relevance to disease pathophysiology. Biol. Mood Anxiety Disord., 2, 2012, 18.
23. Lorenzo, D.N., Badea, A., Davis, J., Hostettler, J., He, J., Zhong, G., Zhuang, X., Bennett, V., A PIK3C3-ankyrin-B-dynactin pathway promotes axonal growth and multiorganelle transport. J. Cell Biol. 207 (2014), 735–752.
24. Maglione, M., Sigrist, S.J., Seeing the forest tree by tree: super-resolution light microscopy meets the neurosciences. Nat. Neurosci. 16 (2013), 790–797.
25. 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. 5 (2003), 626–632.
26. Normand, E.A., Rasband, M.N., Subcellular patterning: axonal domains with specialized structure and function. Dev. Cell 32 (2015), 459–468.
27. Ovesný M., Křížek, P., Borkovec, J., Svindrych, Z., Hagen, G.M., ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30 (2014), 2389–2390.
28. Petersen, J.D., Kaech, S., Banker, G., Selective microtubule-based transport of dendritic membrane proteins arises in concert with axon specification. J. Neurosci. 34 (2014), 4135–4147.
29. Rasband, M.N., The axon initial segment and the maintenance of neuronal polarity. Nat. Rev. Neurosci. 11 (2010), 552–562.
30. Redmond, L., Kashani, A.H., Ghosh, A., Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34 (2002), 999–1010.
31. Schafer, D.P., Jha, S., Liu, F., Akella, T., McCullough, L.D., Rasband, M.N., Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J. Neurosci. 29 (2009), 13242–13254.
32. 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. USA 106 (2009), 17564–17569.
33. 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 136 (2009), 1148–1160.
34. Stephan, R., Goellner, B., Moreno, E., Frank, C.A., Hugenschmidt, T., Genoud, C., Aberle, H., Pielage, J., Hierarchical microtubule organization controls axon caliber and transport and determines synaptic structure and stability. Dev. Cell 33 (2015), 5–21.
35. Sun, X., Wu, Y., Gu, M., Liu, Z., Ma, Y., Li, J., Zhang, Y., Selective filtering defect at the axon initial segment in Alzheimer's disease mouse models. Proc. Natl. Acad. Sci. USA 111 (2014), 14271–14276.
36. Uemoto, Y., Suzuki, S., Terada, N., Ohno, N., Ohno, S., Yamanaka, S., Komada, M., Specific role of the truncated betaIV-spectrin Sigma6 in sodium channel clustering at axon initial segments and nodes of ranvier. J. Biol. Chem. 282 (2007), 6548–6555.
37. 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. 2 (2012), 1546–1553.
38. Westrum, L.E., Gray, E.G., Microtubules and membrane specializations. Brain Res. 105 (1976), 547–550.
39. Winckler, B., Forscher, P., Mellman, I., A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 397 (1999), 698–701.
40. Xu, K., Zhong, G., Zhuang, X., Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339 (2013), 452–456.
41. Yang, Y., Ogawa, Y., Hedstrom, K.L., Rasband, M.N., betaIV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J. Cell Biol. 176 (2007), 509–519.
42. Zhong, G., He, J., Zhou, R., Lorenzo, D., Babcock, H.P., Bennett, V., Zhuang, X., Developmental mechanism of the periodic membrane skeleton in axons. eLife, 3, 2014, e04581.