Microtubule assembly, organization and dynamics in axons and dendrites

During the past decade enormous advances have been made in our understanding of the basic molecular machinery that is involved in the development of neuronal polarity. Far from being mere structural elements, microtubules are emerging as key determinants of neuronal polarity. Here we review the current understanding of the regulation of microtubule assembly, organization and dynamics in axons and dendrites. These studies provide new insight into microtubules' function in neuronal development and their potential contribution to plasticity.

[1]  A. Bretscher,et al.  Microtubule Asymmetry , 2003, Science.

[2]  J. Sanes,et al.  Mammalian SAD Kinases Are Required for Neuronal Polarization , 2005, Science.

[3]  Dylan T Burnette,et al.  Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. , 2008, Developmental cell.

[4]  S. Halpain,et al.  The MAP2/Tau family of microtubule-associated proteins , 2004, Genome Biology.

[5]  P. Baas,et al.  Identification of a Microtubule-associated Motor Protein Essential for Dendritic Differentiation , 1997, The Journal of cell biology.

[6]  N. Leclerc,et al.  HMWMAP2: new perspectives on a pathway to dendritic identity. , 2008, Cell motility and the cytoskeleton.

[7]  J. Gleeson,et al.  Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain , 2006, Nature Neuroscience.

[8]  K. Svoboda,et al.  Diverse Modes of Axon Elaboration in the Developing Neocortex , 2005, PLoS biology.

[9]  R. Vale,et al.  Making more microtubules by severing: a common theme of noncentrosomal microtubule arrays? , 2006, The Journal of cell biology.

[10]  M. Peifer,et al.  Putting the model to the test: are APC proteins essential for neuronal polarity, axon outgrowth, and axon targeting? , 2008, The Journal of cell biology.

[11]  G. Bokoch,et al.  Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? , 2008, Trends in cell biology.

[12]  B. Schnapp,et al.  A Change in the Selective Translocation of the Kinesin-1 Motor Domain Marks the Initial Specification of the Axon , 2006, Neuron.

[13]  A. Ferreira,et al.  The expression of acetylated microtubules during axonal and dendritic growth in cerebellar macroneurons which develop in vitro. , 1989, Brain research. Developmental brain research.

[14]  W. Harris,et al.  Polarization and orientation of retinal ganglion cells in vivo , 2006, Neural Development.

[15]  W. Nelson,et al.  Neurite outgrowth involves adenomatous polyposis coli protein and β-catenin , 2005, Journal of Cell Science.

[16]  Kenneth H. Downing,et al.  Correction: Structure of the αβ tubulin dimer by electron crystallography , 1998, Nature.

[17]  J. Ávila,et al.  End binding protein‐1 (EB1) complements microtubule‐associated protein‐1B during axonogenesis , 2005, Journal of neuroscience research.

[18]  S. Halpain,et al.  The MAP1 family of microtubule-associated proteins , 2006, Genome Biology.

[19]  T. Mitchison,et al.  Microtubule polymerization dynamics. , 1997, Annual review of cell and developmental biology.

[20]  Anna Akhmanova,et al.  Tracking the ends: a dynamic protein network controls the fate of microtubule tips , 2008, Nature Reviews Molecular Cell Biology.

[21]  G. Gundersen.  Evolutionary conservation of microtubule-capture mechanisms , 2002, Nature Reviews Molecular Cell Biology.

[22]  N. K. Wessells,et al.  Axon growth: roles of microfilaments and microtubules. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Goldberg,et al.  Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy , 1986, The Journal of cell biology.

[24]  E. Dent,et al.  Activity-Dependent Dynamic Microtubule Invasion of Dendritic Spines , 2008, The Journal of Neuroscience.

[25]  C. Dotti,et al.  Neuronal Polarity: Vectorial Cytoplasmic Flow Precedes Axon Formation , 1997, Neuron.

[26]  Carlos G. Dotti,et al.  Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis , 2002, Nature Reviews Neuroscience.

[27]  A. Sobel,et al.  The “SCG10-LIke Protein” SCLIP is a novel regulator of axonal branching in hippocampal neurons, unlike SCG10 , 2007, Molecular and Cellular Neuroscience.

[28]  T. Akiyama,et al.  Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. , 2004, Developmental cell.

[29]  E. Stamatakou,et al.  Wnt Regulates Axon Behavior through Changes in Microtubule Growth Directionality: A New Role for Adenomatous Polyposis Coli , 2008, The Journal of Neuroscience.

[30]  J. Garrido,et al.  GSK3 alpha and GSK3 beta are necessary for axon formation , 2007, FEBS letters.

[31]  N. Leclerc,et al.  Interaction of Microtubule-associated Protein-2 and p63 , 2005, Journal of Biological Chemistry.

[32]  A. Hall,et al.  Neuronal polarity is regulated by glycogen synthase kinase-3 (GSK-3β) independently of Akt/PKB serine phosphorylation , 2006, Journal of Cell Science.

[33]  K. Kaibuchi,et al.  PIP3 is involved in neuronal polarization and axon formation , 2004, Journal of neurochemistry.

[34]  A. Kriegstein,et al.  LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages , 2005, The Journal of cell biology.

[35]  C. Sung,et al.  The dynein light chain Tctex-1 has a dynein-independent role in actin remodeling during neurite outgrowth. , 2005, Developmental cell.

[36]  Carlos G. Dotti,et al.  Centrosome localization determines neuronal polarity , 2005, Nature.

[37]  S. Kuroda,et al.  Rac1 and Cdc42 Capture Microtubules through IQGAP1 and CLIP-170 , 2002, Cell.

[38]  N. K. Wessells,et al.  ULTRASTRUCTURE AND FUNCTION OF GROWTH CONES AND AXONS OF CULTURED NERVE CELLS , 1971, The Journal of cell biology.

[39]  N. Hirokawa,et al.  Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization , 2001, The Journal of cell biology.

[40]  吉村 武.  GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity , 2005 .

[41]  O. Reiner,et al.  Reduction of microtubule catastrophe events by LIS1, platelet‐activating factor acetylhydrolase subunit , 1997, The EMBO journal.

[42]  K. Kaibuchi,et al.  CRMP-2 induces axons in cultured hippocampal neurons , 2001, Nature Neuroscience.

[43]  T. Herdegen,et al.  JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length , 2006, The Journal of cell biology.

[44]  M. Kirschner,et al.  Microtubule behavior in the growth cones of living neurons during axon elongation , 1991, The Journal of cell biology.

[45]  G. Drewes,et al.  Microtubule affinity-regulating kinase 2 functions downstream of the PAR-3/PAR-6/atypical PKC complex in regulating hippocampal neuronal polarity. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Etienne-Manneville,et al.  Positioning centrosomes and spindle poles: looking at the periphery to find the centre , 2006, Biology of the cell.

[47]  A. Ferreira,et al.  Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. , 1989, Brain research. Developmental brain research.

[48]  N. Hirokawa,et al.  Delayed Development of Nervous System in Mice Homozygous for Disrupted Microtubule-associated Protein 1B (MAP1B) Gene , 1997, The Journal of cell biology.

[49]  Yimin Zou,et al.  Wnt signaling in neural circuit assembly. , 2008, Annual review of neuroscience.

[50]  Y. Jan,et al.  Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons , 2008, Nature Cell Biology.

[51]  K. Kosik,et al.  Evidence for the Involvement of Tiam1 in Axon Formation , 2001, The Journal of Neuroscience.

[52]  E. Drier,et al.  New Synaptic Bouton Formation Is Disrupted by Misregulation of Microtubule Stability in aPKC Mutants , 2004, Neuron.

[53]  J. Ávila,et al.  Microtubule-associated protein 1B function during normal development, regeneration, and pathological conditions in the nervous system. , 2004, Journal of neurobiology.

[54]  C. Dotti,et al.  The role of local actin instability in axon formation. , 1999, Science.

[55]  Masafumi Nakamura,et al.  Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization , 2001, Current Biology.

[56]  Ronald D Vale,et al.  The Molecular Motor Toolbox for Intracellular Transport , 2003, Cell.

[57]  L. Tsai,et al.  Pyramidal neuron polarity axis is defined at the bipolar stage , 2008, Journal of Cell Science.

[58]  F. Polleux,et al.  New insights into the molecular mechanisms specifying neuronal polarity in vivo , 2008, Current Opinion in Neurobiology.

[59]  S. Kaech,et al.  Cytoskeletal microdifferentiation: A mechanism for organizing morphological plasticity in dendrites , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[60]  G. Banker,et al.  Rapid changes in the distribution of GAP-43 correlate with the expression of neuronal polarity during normal development and under experimental conditions , 1990, The Journal of cell biology.

[61]  N. Hirokawa,et al.  MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction , 2002, The Journal of cell biology.

[62]  J. Sanes,et al.  LKB1 and SAD Kinases Define a Pathway Required for the Polarization of Cortical Neurons , 2007, Cell.

[63]  N. Hirokawa,et al.  Altered microtubule organization in small-calibre axons of mice lacking tau protein , 1994, Nature.

[64]  E. Nogales,et al.  Structural models for the self-assembly and microtubule interactions of gamma-, delta- and epsilon-tubulin. , 2001, Journal of cell science.

[65]  P. Baas,et al.  Depletion of a Microtubule-Associated Motor Protein Induces the Loss of Dendritic Identity , 2000, The Journal of Neuroscience.

[66]  Dawen Cai,et al.  Microtubule Acetylation Promotes Kinesin-1 Binding and Transport , 2006, Current Biology.

[67]  F. Ahmad,et al.  Microtubule fragmentation and partitioning in the axon during collateral branch formation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  A. Koulakoff,et al.  Doublecortin functions at the extremities of growing neuronal processes. , 2003, Cerebral cortex.

[69]  A. Cáceres,et al.  IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity , 2006, Nature Neuroscience.

[70]  M. Kirschner,et al.  The role of microtubule dynamics in growth cone motility and axonal growth , 1995, The Journal of cell biology.

[71]  E. Dent,et al.  Cytoskeletal Dynamics and Transport in Growth Cone Motility and Axon Guidance , 2003, Neuron.

[72]  Niels Galjart,et al.  CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex , 2005, The Journal of cell biology.

[73]  木村 俊秀.  Tubulin and CRMP-2 complex is transported via Kinesin-1 , 2005 .

[74]  E. Nogales.  Structural insights into microtubule function. , 2000, Annual review of biochemistry.

[75]  H. Joshi,et al.  Inhibition of microtubule nucleation at the neuronal centrosome compromises axon growth , 1994, Neuron.

[76]  Dylan T Burnette,et al.  Rho-Dependent Contractile Responses in the Neuronal Growth Cone Are Independent of Classical Peripheral Retrograde Actin Flow , 2003, Neuron.

[77]  Bertrand Fontaine,et al.  Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia , 1999, Nature Genetics.

[78]  K. Kaibuchi,et al.  CRMP-2 binds to tubulin heterodimers to promote microtubule assembly , 2002, Nature Cell Biology.

[79]  L. Qiang,et al.  Regulation of Microtubule Severing by Katanin Subunits during Neuronal Development , 2005, The Journal of Neuroscience.

[80]  G. Gundersen,et al.  Cortical control of microtubule stability and polarization. , 2004, Current opinion in cell biology.

[81]  P. Gaspar,et al.  Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. , 2006, Human molecular genetics.

[82]  L. Qiang,et al.  The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. , 2008, Molecular biology of the cell.

[83]  P. Baas,et al.  Neuronal polarity: microtubules strike back , 2002, Nature Cell Biology.

[84]  E. Mandelkow,et al.  Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. , 2002, Molecular biology of the cell.

[85]  Jacek Gaertig,et al.  The Tubulin Code , 2007, Cell cycle.

[86]  M. Poo,et al.  LKB1/STRAD Promotes Axon Initiation During Neuronal Polarization , 2007, Cell.

[87]  Kozo Kaibuchi,et al.  Neuronal polarity: from extracellular signals to intracellular mechanisms , 2007, Nature Reviews Neuroscience.

[88]  Chris Q Doe,et al.  Microtubule-induced cortical cell polarity. , 2007, Genes & development.

[89]  Yves Grau,et al.  Shaggy, the Homolog of Glycogen Synthase Kinase 3, Controls Neuromuscular Junction Growth in Drosophila , 2004, The Journal of Neuroscience.

[90]  R. Burgoyne,et al.  Synaptic development and microtubule organization , 2004, Cell and Tissue Research.

[91]  Niels Galjart,et al.  CLIPs and CLASPs and cellular dynamics , 2005, Nature Reviews Molecular Cell Biology.

[92]  M. Kirschner,et al.  Beyond self-assembly: From microtubules to morphogenesis , 1986, Cell.

[93]  S. Halpain,et al.  Dynamics and pathology of dendritic spines. , 2005, Progress in brain research.

[94]  P. Salinas,et al.  Inhibition of GSK-3 β leading to the loss of phosphorylated MAP-1 B is an early event in axonal remodelling induced by WNT-7 a or lithium , 1998 .

[95]  Tony Pawson,et al.  Polarity proteins in axon specification and synaptogenesis. , 2005, Developmental cell.

[96]  J. Woodgett,et al.  Essential Roles for GSK-3s and GSK-3-Primed Substrates in Neurotrophin-Induced and Hippocampal Axon Growth , 2006, Neuron.

[97]  K. Kosik,et al.  Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons , 1990, Nature.

[98]  N. Hirokawa,et al.  Defects in Axonal Elongation and Neuronal Migration in Mice with Disrupted tau and map1b Genes , 2000, The Journal of cell biology.

[99]  K. Kosik,et al.  MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. , 1996, Journal of cell science.

[100]  F. Bradke,et al.  The role of the cytoskeleton during neuronal polarization , 2008, Current Opinion in Neurobiology.

[101]  B. Firestein,et al.  Microtubules in Dendritic Spine Development , 2008, The Journal of Neuroscience.

[102]  L. Qiang,et al.  Microtubules cut and run. , 2005, Trends in cell biology.

[103]  G. Banker,et al.  Intracellular organization of hippocampal neurons during the development of neuronal polarity , 1991, Journal of Cell Science.

[104]  N. Mori,et al.  SCG10, a microtubule destabilizing factor, stimulates the neurite outgrowth by modulating microtubule dynamics in rat hippocampal primary cultured neurons. , 2006, Journal of neurobiology.

[105]  R. Maccioni,et al.  Microtubule-Associated Protein 1B Interaction with Tubulin Tyrosine Ligase Contributes to the Control of Microtubule Tyrosination , 2007, Developmental Neuroscience.

[106]  Li-Huei Tsai,et al.  Trekking across the Brain: The Journey of Neuronal Migration , 2007, Cell.

[107]  E. Nogales,et al.  Refined structure of alpha beta-tubulin at 3.5 A resolution. , 2001, Journal of molecular biology.

[108]  W. Nelson,et al.  Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. , 2008, Seminars in cell & developmental biology.

[109]  K. Kaibuchi,et al.  GSK-3β Regulates Phosphorylation of CRMP-2 and Neuronal Polarity , 2005, Cell.

[110]  Tau impacts on growth-factor-stimulated actin remodeling , 2007, Journal of Cell Science.

[111]  R. Luduena.  Multiple forms of tubulin: different gene products and covalent modifications. , 1998, International review of cytology.

[112]  G. Davis,et al.  Drosophila Futsch/22C10 Is a MAP1B-like Protein Required for Dendritic and Axonal Development , 2000, Neuron.

[113]  Dawen Cai,et al.  Tubulin modifications and their cellular functions. , 2008, Current opinion in cell biology.

[114]  J. Quigley,et al.  The extracellular matrix of normal chick embryo fibroblasts: its effect on transformed chick fibroblasts and its proteolytic degradation by the transformants , 1985, The Journal of cell biology.

[115]  G. Banker,et al.  The establishment of polarity by hippocampal neurons in culture , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[116]  F. Bradke,et al.  Microtubule stabilization specifies initial neuronal polarization , 2008, The Journal of cell biology.

[117]  K. Kaibuchi,et al.  Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. , 2008, Developmental cell.

[118]  R. Burgoyne,et al.  Synaptic organisation and neuron microtubule distribution , 2004, Cell and Tissue Research.

[119]  G. Davis,et al.  Drosophila Futsch Regulates Synaptic Microtubule Organization and Is Necessary for Synaptic Growth , 2000, Neuron.

[120]  C. Hoogenraad,et al.  Microtubule plus-end tracking proteins in differentiated mammalian cells. , 2008, The international journal of biochemistry & cell biology.

[121]  V. Budnik,et al.  The Drosophila Wnt, Wingless, Provides an Essential Signal for Pre- and Postsynaptic Differentiation , 2002, Cell.

[122]  Mitsuko Watabe-Uchida,et al.  The Rac Activator DOCK7 Regulates Neuronal Polarity through Local Phosphorylation of Stathmin/Op18 , 2006, Neuron.

[123]  A. Sobel,et al.  Two separate motifs cooperate to target stathmin-related proteins to the Golgi complex , 2005, Journal of Cell Science.

[124]  E. Morrison,et al.  EB1 identifies sites of microtubule polymerisation during neurite development. , 2002, Brain research. Molecular brain research.

[125]  M. Black,et al.  Newly assembled microtubules are concentrated in the proximal and distal regions of growing axons , 1992, The Journal of cell biology.

[126]  Mark Ellisman,et al.  JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. , 2003, Developmental cell.

[127]  S. Dedhar,et al.  NGF-Induced Axon Growth Is Mediated by Localized Inactivation of GSK-3β and Functions of the Microtubule Plus End Binding Protein APC , 2004, Neuron.

[128]  M. Chen,et al.  EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration , 2004, Nature Cell Biology.

[129]  J. Tuszynski,et al.  The evolution of the structure of tubulin and its potential consequences for the role and function of microtubules in cells and embryos. , 2006, The International journal of developmental biology.

[130]  O. Steward,et al.  Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[131]  Mustafa Sahin,et al.  Tuberous sclerosis complex proteins control axon formation. , 2008, Genes & development.

[132]  G. Gundersen,et al.  Cell biology (Communication arising): Tubulin acetylation and cell motility , 2003, Nature.

[133]  Y. Li,et al.  Composite microtubules of the axon: quantitative analysis of tyrosinated and acetylated tubulin along individual axonal microtubules. , 1993, Journal of cell science.

[134]  Xiaoxin X. Wang,et al.  PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone , 2005, Journal of Cell Science.

[135]  W. Snider,et al.  GSK-3β and Microtubule Assembly in Axons , 2005, Science.

[136]  S. Etienne-Manneville,et al.  Cdc42 - the centre of polarity , 2004, Journal of Cell Science.

[137]  L. Westrum,et al.  Microtubules, dendritic spines and spine apparatuses , 2004, Cell and Tissue Research.

[138]  H. Wässle,et al.  Map1b Is Required for Axon Guidance and Is Involved in the Development of the Central and Peripheral Nervous System , 2000, The Journal of cell biology.

[139]  L. Van Aelst,et al.  The role of the Rho GTPases in neuronal development. , 2005, Genes & development.

[140]  J. Zmuda,et al.  The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. , 1998, Cell motility and the cytoskeleton.

[141]  H. Barra,et al.  Posttranslational tyrosination/detyrosination of tubulin , 2008, Molecular Neurobiology.

[142]  P. Baas,et al.  Distribution of the microtubule-related protein ninein in developing neurons , 2004, Neuropharmacology.

[143]  Kenneth H. Downing,et al.  Structure of the αβ tubulin dimer by electron crystallography , 1998, Nature.

[144]  W. Witke,et al.  RhoA/ROCK regulation of neuritogenesis via profilin IIa–mediated control of actin stability , 2003, The Journal of cell biology.

[145]  L. Luo.  RHO GTPASES in neuronal morphogenesis , 2000, Nature Reviews Neuroscience.

[146]  A. Hyman,et al.  Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3β phosphorylation , 2001, Current Biology.

[147]  C. Hoogenraad,et al.  Dynamic Microtubules Regulate Dendritic Spine Morphology and Synaptic Plasticity , 2009, Neuron.

[148]  K. Kalil,et al.  Reorganization and Movement of Microtubules in Axonal Growth Cones and Developing Interstitial Branches , 1999, The Journal of Neuroscience.

[149]  Nobutaka Hirokawa,et al.  Intracellular Transport and Kinesin Superfamily Proteins, Kifs: Structure, Function, and Dynamics , 2022 .

[150]  G. Gundersen,et al.  Stabilization and post‐translational modification of microtubules during cellular morphogenesis , 1991 .

[151]  Lily Yeh Jan,et al.  The Control of Dendrite Development , 2003, Neuron.

[152]  G. Danuser,et al.  Coordination of actin filament and microtubule dynamics during neurite outgrowth. , 2008, Developmental cell.

[153]  E. Shooter,et al.  Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors , 1985, The Journal of cell biology.

[154]  M. Black,et al.  Individual microtubules in the axon consist of domains that differ in both composition and stability , 1990, The Journal of cell biology.

[155]  P. Bondallaz,et al.  Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth. , 2004, Journal of neurobiology.

[156]  Chris I. De Zeeuw,et al.  CLASPs Are CLIP-115 and -170 Associating Proteins Involved in the Regional Regulation of Microtubule Dynamics in Motile Fibroblasts , 2001, Cell.

[157]  W. Snider,et al.  Cell biology. GSK-3beta and microtubule assembly in axons. , 2005, Science.

[158]  Y. Jan,et al.  Hippocampal Neuronal Polarity Specified by Spatially Localized mPar3/mPar6 and PI 3-Kinase Activity , 2003, Cell.

[159]  D. Srivastava,et al.  Not Just Actin? A Role for Dynamic Microtubules in Dendritic Spines , 2009, Neuron.

[160]  M. Daniels.  COLCHICINE INHIBITION OF NERVE FIBER FORMATION IN VITRO , 1972, The Journal of cell biology.

[161]  Nancy Ratner,et al.  Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin‐based motility , 2002, The EMBO journal.

[162]  L. Wilson,et al.  Stathmin family protein SCG10 differentially regulates the plus and minus end dynamics of microtubules at steady state in vitro: implications for its role in neurite outgrowth. , 2007, Biochemistry.

[163]  E. Rugarli,et al.  Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. , 2004, Human molecular genetics.

[164]  E. Nogales.  Structural insight into microtubule function. , 2001, Annual review of biophysics and biomolecular structure.

[165]  S Inoué,et al.  1. EARLY HISTORY: THE DYNAMIC EQUILIBRIUM MODEL , 1995 .

[166]  H. Erickson.  γ-tubulin nucleation: template or protofilament? , 2000, Nature Cell Biology.

[167]  Y. Rao,et al.  Both the Establishment and the Maintenance of Neuronal Polarity Require Active Mechanisms Critical Roles of GSK-3β and Its Upstream Regulators , 2005, Cell.

[168]  J. Solowska,et al.  Axonal Growth Is Sensitive to the Levels of Katanin, a Protein That Severs Microtubules , 2004, The Journal of Neuroscience.

[169]  P. Gordon-Weeks,et al.  The MAP kinase pathway is upstream of the activation of GSK3β that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth , 2005, Molecular and Cellular Neuroscience.

[170]  J. Chilton,et al.  Targeting of the F-actin-binding protein drebrin by the microtubule plus-tip protein EB3 is required for neuritogenesis , 2008, Nature Cell Biology.

[171]  Timothy J. Mitchison,et al.  Microtubule dynamic instability , 2006, Current Biology.

[172]  Mitsuko Watabe-Uchida,et al.  Supplemental Experimental Procedures , 2022 .

[173]  堀口 かおり.  Transport of PIP3 by GAKIN, a kinesin-3 family protein, regulates neuronal cell polarity , 2007 .

[174]  Y. Jan,et al.  APC and GSK-3β Are Involved in mPar3 Targeting to the Nascent Axon and Establishment of Neuronal Polarity , 2004, Current Biology.

[175]  Kozo Kaibuchi,et al.  [Neuronal polarity]. , 2008, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[176]  E. Rugarli,et al.  Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. , 2002, Human molecular genetics.

[177]  A. Brown,et al.  Sites of microtubule stabilization for the axon , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[178]  K. Inokuchi,et al.  The microtubule destabilizer stathmin mediates the development of dendritic arbors in neuronal cells , 2007, Journal of Cell Science.

[179]  C. Wierenga,et al.  Plasticity of Polarization: Changing Dendrites into Axons in Neurons Integrated in Neuronal Circuits , 2008, Current Biology.

[180]  E. Salmon,et al.  Fluorescent speckle microscopy of microtubules: how low can you go? , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[181]  J. Ávila,et al.  Evidence for the role of MAP1B in axon formation. , 2001, Molecular biology of the cell.

[182]  R. Vallee,et al.  Cytoplasmic Dynein and LIS1 Are Required for Microtubule Advance during Growth Cone Remodeling and Fast Axonal Outgrowth , 2007, The Journal of Neuroscience.

[183]  M. Vitek,et al.  Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. , 2001, Journal of cell science.

[184]  K. Broadie,et al.  The Hereditary Spastic Paraplegia Gene, spastin, Regulates Microtubule Stability to Modulate Synaptic Structure and Function , 2004, Current Biology.

[185]  K. Kosik,et al.  Suppression of MAP2 in cultured cerebeller macroneurons inhibits minor neurite formation , 1992, Neuron.

[186]  N. Hirokawa,et al.  Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head , 2003, The Journal of cell biology.

[187]  G. Morfini,et al.  Regulation of membrane expansion at the nerve growth cone , 2003, Journal of Cell Science.

[188]  G. Gundersen,et al.  Kinesin Is a Candidate for Cross-bridging Microtubules and Intermediate Filaments , 1998, The Journal of Biological Chemistry.

[189]  D. Bentley,et al.  Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ , 1989, The Journal of cell biology.

[190]  R. Hartman,et al.  Deletion of the n-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory , 2003, Neuroscience.

[191]  Y. Li,et al.  Microtubule assembly and turnover in growing axons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[192]  L. Qiang,et al.  Tau Protects Microtubules in the Axon from Severing by Katanin , 2006, The Journal of Neuroscience.

[193]  V. Centonze,et al.  Microtubule nucleation and release from the neuronal centrosome , 1993, The Journal of cell biology.

[194]  M. Hoshino,et al.  PAR-6–PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1 , 2005, Nature Cell Biology.

[195]  P. Baas,et al.  Slow axonal transport and the genesis of neuronal morphology. , 2004, Journal of neurobiology.

[196]  N. Hirokawa,et al.  Kinesin Superfamily Protein 2A (KIF2A) Functions in Suppression of Collateral Branch Extension , 2003, Cell.

[197]  T. Deerinck,et al.  Spinophilin Facilitates Dephosphorylation of Doublecortin by PP1 to Mediate Microtubule Bundling at the Axonal Wrist , 2007, Cell.

[198]  P. Baas,et al.  An Essential Role for Katanin in Severing Microtubules in the Neuron , 1999, The Journal of cell biology.

[199]  A. Alonso,et al.  Signaling Mechanisms Underlying Reversible, Activity-Dependent Dendrite Formation , 2002, Neuron.

[200]  H. Barra,et al.  Tyrosinated and detyrosinated microtubules in axonal processes of cerebellar macroneurons grown in culture , 1991, Journal of neuroscience research.

[201]  S. Brady,et al.  Activity-Driven Dendritic Remodeling Requires Microtubule-Associated Protein 1A , 2005, Current Biology.

[202]  E. Nogales,et al.  Structural models for the self-assembly and microtubule interactions of γ-, δ-and ε-tubulin , 2022 .

[203]  C. Hoogenraad,et al.  LIS1, CLIP-170's Key to the Dynein/Dynactin Pathway , 2002, Molecular and Cellular Biology.