Kinesin-13 and Tubulin Posttranslational Modifications Regulate Microtubule Growth in Axon Regeneration

Developmental Cell - Tập 23 - Trang 716-728 - 2012
Anindya Ghosh-Roy1, Alexandr Goncharov1,2, Yishi Jin1,2, Andrew D. Chisholm1
1Division of Biological Sciences, Section of Neurobiology, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA
2Howard Hughes Medical Institute

Tài liệu tham khảo

Ahmad, 1993, Regional differences in microtubule dynamics in the axon, J. Neurosci., 13, 856, 10.1523/JNEUROSCI.13-02-00856.1993 Andrews, 2004, Aurora B regulates MCAK at the mitotic centromere, Dev. Cell, 6, 253, 10.1016/S1534-5807(04)00025-5 Baas, 2005, Neuronal microtubules: when the MAP is the roadblock, Trends Cell Biol., 15, 183, 10.1016/j.tcb.2005.02.001 Baas, 1993, Sites of microtubule stabilization for the axon, J. Neurosci., 13, 2177, 10.1523/JNEUROSCI.13-05-02177.1993 El Bejjani, 2012, Notch signaling inhibits axon regeneration, Neuron, 73, 268, 10.1016/j.neuron.2011.11.017 Bounoutas, 2011, Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway, Proc. Natl. Acad. Sci. USA, 108, 3982, 10.1073/pnas.1101360108 Bradke, 2000, Differentiated neurons retain the capacity to generate axons from dendrites, Curr. Biol., 10, 1467, 10.1016/S0960-9822(00)00807-1 Bradke, 2012, Assembly of a new growth cone after axotomy: the precursor to axon regeneration, Nat. Rev. Neurosci., 13, 183, 10.1038/nrn3176 Cassimeris, 2002, The oncoprotein 18/stathmin family of microtubule destabilizers, Curr. Opin. Cell Biol., 14, 18, 10.1016/S0955-0674(01)00289-7 Cassimeris, 1988, Real-time observations of microtubule dynamic instability in living cells, J. Cell Biol., 107, 2223, 10.1083/jcb.107.6.2223 Chalfie, 1979, Organization of neuronal microtubules in the nematode Caenorhabditis elegans, J. Cell Biol., 82, 278, 10.1083/jcb.82.1.278 Chen, 2011, Axon regeneration mechanisms: insights from C. elegans, Trends Cell Biol., 21, 577, 10.1016/j.tcb.2011.08.003 Chen, 2011, Axon regeneration pathways identified by systematic genetic screening in C. elegans, Neuron, 71, 1043, 10.1016/j.neuron.2011.07.009 Dehmelt, 2003, The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation, J. Neurosci., 23, 9479, 10.1523/JNEUROSCI.23-29-09479.2003 Desai, 1997, Microtubule polymerization dynamics, Annu. Rev. Cell Dev. Biol., 13, 83, 10.1146/annurev.cellbio.13.1.83 Desai, 1999, Kin I kinesins are microtubule-destabilizing enzymes, Cell, 96, 69, 10.1016/S0092-8674(00)80960-5 Duggan, 1998, Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes, Development, 125, 4107, 10.1242/dev.125.20.4107 Ems-McClung, 2007, The interplay of the N- and C-terminal domains of MCAK control microtubule depolymerization activity and spindle assembly, Mol. Biol. Cell, 18, 282, 10.1091/mbc.e06-08-0724 Erck, 2005, A vital role of tubulin-tyrosine-ligase for neuronal organization, Proc. Natl. Acad. Sci. USA, 102, 7853, 10.1073/pnas.0409626102 Erez, 2008, Local self-assembly mechanisms underlie the differential transformation of the proximal and distal cut axonal ends into functional and aberrant growth cones, J. Comp. Neurol., 507, 1019, 10.1002/cne.21522 Ertürk, 2007, Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration, J. Neurosci., 27, 9169, 10.1523/JNEUROSCI.0612-07.2007 Fernandez-Gonzalez, 2002, Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1, Science, 295, 1904, 10.1126/science.1068912 Finney, 1990, The unc-86 gene product couples cell lineage and cell identity in C. elegans, Cell, 63, 895, 10.1016/0092-8674(90)90493-X Gabel, 2008, Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans, Development, 135, 1129, 10.1242/dev.013995 Ghosh-Roy, 2010, Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase, J. Neurosci., 30, 3175, 10.1523/JNEUROSCI.5464-09.2010 Gomis-Rüth, 2008, Plasticity of polarization: changing dendrites into axons in neurons integrated in neuronal circuits, Curr. Biol., 18, 992, 10.1016/j.cub.2008.06.026 Goodwin, 2012, Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons, J. Neurosci., 32, 8158, 10.1523/JNEUROSCI.0251-12.2012 Guillaud, 1998, STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells, J. Cell Biol., 142, 167, 10.1083/jcb.142.1.167 Hammarlund, 2009, Axon regeneration requires a conserved MAP kinase pathway, Science, 323, 802, 10.1126/science.1165527 Hao, 2011, Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments, Nat. Cell Biol., 13, 790, 10.1038/ncb2268 Harris, 2000, Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases, Mol. Cell. Neurosci., 16, 578, 10.1006/mcne.2000.0900 Helenius, 2006, The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends, Nature, 441, 115, 10.1038/nature04736 Hellal, 2011, Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury, Science, 331, 928, 10.1126/science.1201148 Hendricks, 2009, PHR regulates growth cone pausing at intermediate targets through microtubule disassembly, J. Neurosci., 29, 6593, 10.1523/JNEUROSCI.1115-09.2009 Hirai, 2011, Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-Jun N-terminal kinase pathway, J. Neurosci., 31, 6468, 10.1523/JNEUROSCI.5038-10.2011 Honnappa, 2009, An EB1-binding motif acts as a microtubule tip localization signal, Cell, 138, 366, 10.1016/j.cell.2009.04.065 Howard, 2007, Microtubule polymerases and depolymerases, Curr. Opin. Cell Biol., 19, 31, 10.1016/j.ceb.2006.12.009 Itoh, 2009, Impaired regenerative response of primary sensory neurons in ZPK/DLK gene-trap mice, Biochem. Biophys. Res. Commun., 383, 258, 10.1016/j.bbrc.2009.04.009 Janke, 2010, Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton, Trends Neurosci., 33, 362, 10.1016/j.tins.2010.05.001 Kimura, 2010, Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs), J. Biol. Chem., 285, 22936, 10.1074/jbc.C110.128280 Lan, 2004, Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity, Curr. Biol., 14, 273, 10.1016/j.cub.2004.01.055 Lewcock, 2007, The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics, Neuron, 56, 604, 10.1016/j.neuron.2007.09.009 Maney, 2001, Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin, J. Biol. Chem., 276, 34753, 10.1074/jbc.M106626200 Maniar, 2012, UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting, Nat. Neurosci., 15, 48, 10.1038/nn.2970 Mitchison, 1984, Dynamic instability of microtubule growth, Nature, 312, 237, 10.1038/312237a0 Montenegro Gouveia, 2010, In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends, Curr. Biol., 20, 1717, 10.1016/j.cub.2010.08.020 Nakata, 2005, Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development, Cell, 120, 407, 10.1016/j.cell.2004.12.017 Nix, 2011, Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways, Proc. Natl. Acad. Sci. USA, 108, 10738, 10.1073/pnas.1104830108 O’Hagan, 2011, The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans, Curr Biol., 21, 1685, 10.1016/j.cub.2011.08.049 Paturle-Lafanechère, 1991, Characterization of a major brain tubulin variant which cannot be tyrosinated, Biochemistry, 30, 10523, 10.1021/bi00107a022 Paturle-Lafanechère, 1994, Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies, J. Cell Sci., 107, 1529, 10.1242/jcs.107.6.1529 Peris, 2009, Motor-dependent microtubule disassembly driven by tubulin tyrosination, J. Cell Biol., 185, 1159, 10.1083/jcb.200902142 Pinan-Lucarre, 2012, The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans, PLoS Biol., 10, e1001331, 10.1371/journal.pbio.1001331 Ramon y Cajal, S. (1928). Cajal’s Degeneration and Regeneration of the Nervous System, J. Defelipe and E.G. Jones, eds. (R.M. May, trans.) (New York, NY: Oxford University Press). Rogowski, 2010, A family of protein-deglutamylating enzymes associated with neurodegeneration, Cell, 143, 564, 10.1016/j.cell.2010.10.014 Samara, 2010, Large-scale in vivo femtosecond laser neurosurgery screen reveals small-molecule enhancer of regeneration, Proc. Natl. Acad. Sci. USA, 107, 18342, 10.1073/pnas.1005372107 Sengottuvel, 2011, Taxol facilitates axon regeneration in the mature CNS, J. Neurosci., 31, 2688, 10.1523/JNEUROSCI.4885-10.2011 Shin, 2012, Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration, Neuron, 74, 1015, 10.1016/j.neuron.2012.04.028 Srayko, 2005, Identification and characterization of factors required for microtubule growth and nucleation in the early C. elegans embryo, Dev. Cell, 9, 223, 10.1016/j.devcel.2005.07.003 Stepanova, 2003, Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein), J. Neurosci., 23, 2655, 10.1523/JNEUROSCI.23-07-02655.2003 Stepanova, 2010, History-dependent catastrophes regulate axonal microtubule behavior, Curr. Biol., 20, 1023, 10.1016/j.cub.2010.04.024 Suter, 2004, Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering, Curr. Biol., 14, 1194, 10.1016/j.cub.2004.06.049 Usher, 2010, A chemical screen identifies novel compounds that overcome glial-mediated inhibition of neuronal regeneration, J. Neurosci., 30, 4693, 10.1523/JNEUROSCI.0302-10.2010 Vale, 1997, The design plan of kinesin motors, Annu. Rev. Cell Dev. Biol., 13, 745, 10.1146/annurev.cellbio.13.1.745 Witte, 2008, The role of the cytoskeleton during neuronal polarization, Curr. Opin. Neurobiol., 18, 479, 10.1016/j.conb.2008.09.019 Witte, 2008, Microtubule stabilization specifies initial neuronal polarization, J. Cell Biol., 180, 619, 10.1083/jcb.200707042 Wu, 2007, Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching, Proc. Natl. Acad. Sci. USA, 104, 15132, 10.1073/pnas.0707001104 Xiong, 2010, Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury, J. Cell Biol., 191, 211, 10.1083/jcb.201006039 Yan, 2009, The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration, Cell, 138, 1005, 10.1016/j.cell.2009.06.023 Yu, 1994, Microtubule fragmentation and partitioning in the axon during collateral branch formation, J. Neurosci., 14, 5872, 10.1523/JNEUROSCI.14-10-05872.1994 Zhang, 2007, Aurora B phosphorylates multiple sites on mitotic centromere-associated kinesin to spatially and temporally regulate its function, Mol. Biol. Cell, 18, 3264, 10.1091/mbc.e07-01-0086