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

Developmental Cell

Volumn 23, Issue 4, 2012, Pages 716-728

  Ghosh Roy, Anindya ^a   Goncharov, Alexandr ^a,b   Jin, Yishi ^a,b   Chisholm, Andrew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; CARBOXYPEPTIDASE; KINESIN; KINESIN 13; MITOGEN ACTIVATED PROTEIN KINASE; TUBULIN; UNCLASSIFIED DRUG;

ARTICLE; AXONAL INJURY; CAENORHABDITIS ELEGANS; CYTOSKELETON; CYTOSOL; DOWN REGULATION; IMAGING SYSTEM; IN VIVO STUDY; MICROTUBULE; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REGULATORY MECHANISM; UPREGULATION;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; KINESIN; MICROTUBULES; NERVE REGENERATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TUBULIN;

CAENORHABDITIS ELEGANS;

EID: 84867725772     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.08.010     Document Type: Article

References (71)

1. Ahmad F.J., Pienkowski T.P., Baas P.W. Regional differences in microtubule dynamics in the axon. J. Neurosci. 1993, 13:856-866.
2. Andrews P.D., Ovechkina Y., Morrice N., Wagenbach M., Duncan K., Wordeman L., Swedlow J.R. Aurora B regulates MCAK at the mitotic centromere. Dev. Cell 2004, 6:253-268.
3. Baas P.W., Qiang L. Neuronal microtubules: when the MAP is the roadblock. Trends Cell Biol. 2005, 15:183-187.
4. Baas P.W., Ahmad F.J., Pienkowski T.P., Brown A., Black M.M. Sites of microtubule stabilization for the axon. J. Neurosci. 1993, 13:2177-2185.
5. El Bejjani R., Hammarlund M. Notch signaling inhibits axon regeneration. Neuron 2012, 73:268-278.
6. Bounoutas A., Kratz J., Emtage L., Ma C., Nguyen K.C., Chalfie M. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. Proc. Natl. Acad. Sci. USA 2011, 108:3982-3987.
7. Bradke F., Dotti C.G. Differentiated neurons retain the capacity to generate axons from dendrites. Curr. Biol. 2000, 10:1467-1470.
8. Bradke F., Fawcett J.W., Spira M.E. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 2012, 13:183-193.
9. Cassimeris L. The oncoprotein 18/stathmin family of microtubule destabilizers. Curr. Opin. Cell Biol. 2002, 14:18-24.
10. Cassimeris L., Pryer N.K., Salmon E.D. Real-time observations of microtubule dynamic instability in living cells. J. Cell Biol. 1988, 107:2223-2231.
11. Chalfie M., Thomson J.N. Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J. Cell Biol. 1979, 82:278-289.
12. Chen L., Chisholm A.D. Axon regeneration mechanisms: insights from C. elegans. Trends Cell Biol. 2011, 21:577-584.
13. Chen L., Wang Z., Ghosh-Roy A., Hubert T., Yan D., O'Rourke S., Bowerman B., Wu Z., Jin Y., Chisholm A.D. Axon regeneration pathways identified by systematic genetic screening in C. elegans. Neuron 2011, 71:1043-1057.
14. Dehmelt L., Smart F.M., Ozer R.S., Halpain S. The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J. Neurosci. 2003, 23:9479-9490.
15. Desai A., Mitchison T.J. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 1997, 13:83-117.
16. Desai A., Verma S., Mitchison T.J., Walczak C.E. Kin I kinesins are microtubule-destabilizing enzymes. Cell 1999, 96:69-78.
17. Duggan A., Ma C., Chalfie M. Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 1998, 125:4107-4119.
18. Ems-McClung S.C., Hertzer K.M., Zhang X., Miller M.W., Walczak C.E. The interplay of the N- and C-terminal domains of MCAK control microtubule depolymerization activity and spindle assembly. Mol. Biol. Cell 2007, 18:282-294.
19. Erck C., Peris L., Andrieux A., Meissirel C., Gruber A.D., Vernet M., Schweitzer A., Saoudi Y., Pointu H., Bosc C., et al. A vital role of tubulin-tyrosine-ligase for neuronal organization. Proc. Natl. Acad. Sci. USA 2005, 102:7853-7858.
20. Erez H., Spira M.E. 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. 2008, 507:1019-1030.
21. Ertürk A., Hellal F., Enes J., Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J. Neurosci. 2007, 27:9169-9180.
22. Fernandez-Gonzalez A., La Spada A.R., Treadaway J., Higdon J.C., Harris B.S., Sidman R.L., Morgan J.I., Zuo J. Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 2002, 295:1904-1906.
23. Finney M., Ruvkun G. The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 1990, 63:895-905.
24. Gabel C.V., Antoine F., Chuang C.F., Samuel A.D., Chang C. Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 2008, 135:1129-1136.
25. Ghosh-Roy A., Wu Z., Goncharov A., Jin Y., Chisholm A.D. Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J. Neurosci. 2010, 30:3175-3183.
26. Gomis-Rüth S., Wierenga C.J., Bradke F. Plasticity of polarization: changing dendrites into axons in neurons integrated in neuronal circuits. Curr. Biol. 2008, 18:992-1000.
27. Goodwin P.R., Sasaki J.M., Juo P. Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons. J. Neurosci. 2012, 32:8158-8172.
28. Guillaud L., Bosc C., Fourest-Lieuvin A., Denarier E., Pirollet F., Lafanechère L., Job D. STOP proteins are responsible for the high degree of microtubule stabilization observed in neuronal cells. J. Cell Biol. 1998, 142:167-179.
29. Hammarlund M., Nix P., Hauth L., Jorgensen E.M., Bastiani M. Axon regeneration requires a conserved MAP kinase pathway. Science 2009, 323:802-806.
30. Hao L., Thein M., Brust-Mascher I., Civelekoglu-Scholey G., Lu Y., Acar S., Prevo B., Shaham S., Scholey J.M. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat. Cell Biol. 2011, 13:790-798.
31. Harris A., Morgan J.I., Pecot M., Soumare A., Osborne A., Soares H.D. Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases. Mol. Cell. Neurosci. 2000, 16:578-596.
32. Helenius J., Brouhard G., Kalaidzidis Y., Diez S., Howard J. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends. Nature 2006, 441:115-119.
33. Hellal F., Hurtado A., Ruschel J., Flynn K.C., Laskowski C.J., Umlauf M., Kapitein L.C., Strikis D., Lemmon V., Bixby J., et al. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331:928-931.
34. Hendricks M., Jesuthasan S. PHR regulates growth cone pausing at intermediate targets through microtubule disassembly. J. Neurosci. 2009, 29:6593-6598.
35. Hirai S., Banba Y., Satake T., Ohno S. 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. 2011, 31:6468-6480.
36. Honnappa S., Gouveia S.M., Weisbrich A., Damberger F.F., Bhavesh N.S., Jawhari H., Grigoriev I., van Rijssel F.J., Buey R.M., Lawera A., et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138:366-376.
37. Howard J., Hyman A.A. Microtubule polymerases and depolymerases. Curr. Opin. Cell Biol. 2007, 19:31-35.
38. Itoh A., Horiuchi M., Bannerman P., Pleasure D., Itoh T. Impaired regenerative response of primary sensory neurons in ZPK/DLK gene-trap mice. Biochem. Biophys. Res. Commun. 2009, 383:258-262.
39. Janke C., Kneussel M. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 2010, 33:362-372.
40. Kimura Y., Kurabe N., Ikegami K., Tsutsumi K., Konishi Y., Kaplan O.I., Kunitomo H., Iino Y., Blacque O.E., Setou M. Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J. Biol. Chem. 2010, 285:22936-22941.
41. Lan W., Zhang X., Kline-Smith S.L., Rosasco S.E., Barrett-Wilt G.A., Shabanowitz J., Hunt D.F., Walczak C.E., Stukenberg P.T. Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity. Curr. Biol. 2004, 14:273-286.
42. Lewcock J.W., Genoud N., Lettieri K., Pfaff S.L. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 2007, 56:604-620.
43. Maney T., Wagenbach M., Wordeman L. Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin. J. Biol. Chem. 2001, 276:34753-34758.
44. 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.
45. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature 1984, 312:237-242.
46. Montenegro Gouveia S., Leslie K., Kapitein L.C., Buey R.M., Grigoriev I., Wagenbach M., Smal I., Meijering E., Hoogenraad C.C., Wordeman L., et al. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr. Biol. 2010, 20:1717-1722.
47. Nakata K., Abrams B., Grill B., Goncharov A., Huang X., Chisholm A.D., Jin Y. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 2005, 120:407-420.
48. Nix P., Hisamoto N., Matsumoto K., Bastiani M. Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. Proc. Natl. Acad. Sci. USA 2011, 108:10738-10743.
49. O'Hagan R., Piasecki B.P., Silva M., Phirke P., Nguyen K.C., Hall D.H., Swoboda P., Barr M.M. The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol. 2011, 21:1685-1694.
50. Paturle-Lafanechère L., Eddé B., Denoulet P., Van Dorsselaer A., Mazarguil H., Le Caer J.P., Wehland J., Job D. Characterization of a major brain tubulin variant which cannot be tyrosinated. Biochemistry 1991, 30:10523-10528.
51. Paturle-Lafanechère L., Manier M., Trigault N., Pirollet F., Mazarguil H., Job D. Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stable microtubule assemblies. J. Cell Sci. 1994, 107:1529-1543.
52. Peris L., Wagenbach M., Lafanechère L., Brocard J., Moore A.T., Kozielski F., Job D., Wordeman L., Andrieux A. Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. Cell Biol. 2009, 185:1159-1166.
53. Pinan-Lucarre B., Gabel C.V., Reina C.P., Hulme S.E., Shevkoplyas S.S., Slone R.D., Xue J., Qiao Y., Weisberg S., Roodhouse K., et al. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol. 2012, 10:e1001331.
54. 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).
55. Rogowski K., van Dijk J., Magiera M.M., Bosc C., Deloulme J.C., Bosson A., Peris L., Gold N.D., Lacroix B., Grau M.B., et al. A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 2010, 143:564-578.
56. Samara C., Rohde C.B., Gilleland C.L., Norton S., Haggarty S.J., Yanik M.F. Large-scale in vivo femtosecond laser neurosurgery screen reveals small-molecule enhancer of regeneration. Proc. Natl. Acad. Sci. USA 2010, 107:18342-18347.
57. Sengottuvel V., Leibinger M., Pfreimer M., Andreadaki A., Fischer D. Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 2011, 31:2688-2699.
58. Shin J.E., Cho Y., Beirowski B., Milbrandt J., Cavalli V., DiAntonio A. Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 2012, 74:1015-1022.
59. Srayko M., Kaya A., Stamford J., Hyman A.A. Identification and characterization of factors required for microtubule growth and nucleation in the early C. elegans embryo. Dev. Cell 2005, 9:223-236.
60. Stepanova T., Slemmer J., Hoogenraad C.C., Lansbergen G., Dortland B., De Zeeuw C.I., Grosveld F., van Cappellen G., Akhmanova A., Galjart N. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 2003, 23:2655-2664.
61. Stepanova T., Smal I., van Haren J., Akinci U., Liu Z., Miedema M., Limpens R., van Ham M., van der Reijden M., Poot R., et al. History-dependent catastrophes regulate axonal microtubule behavior. Curr. Biol. 2010, 20:1023-1028.
62. Suter D.M., Schaefer A.W., Forscher P. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 2004, 14:1194-1199.
63. Usher L.C., Johnstone A., Ertürk A., Hu Y., Strikis D., Wanner I.B., Moorman S., Lee J.W., Min J., Ha H.H., et al. A chemical screen identifies novel compounds that overcome glial-mediated inhibition of neuronal regeneration. J. Neurosci. 2010, 30:4693-4706.
64. Vale R.D., Fletterick R.J. The design plan of kinesin motors. Annu. Rev. Cell Dev. Biol. 1997, 13:745-777.
65. Witte H., Bradke F. The role of the cytoskeleton during neuronal polarization. Curr. Opin. Neurobiol. 2008, 18:479-487.
66. Witte H., Neukirchen D., Bradke F. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 2008, 180:619-632.
67. Wu Z., Ghosh-Roy A., Yanik M.F., Zhang J.Z., Jin Y., Chisholm A.D. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl. Acad. Sci. USA 2007, 104:15132-15137.
68. Xiong X., Wang X., Ewanek R., Bhat P., Diantonio A., Collins C.A. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 2010, 191:211-223.
69. Yan D., Wu Z., Chisholm A.D., Jin Y. The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 2009, 138:1005-1018.
70. Yu W., Ahmad F.J., Baas P.W. Microtubule fragmentation and partitioning in the axon during collateral branch formation. J. Neurosci. 1994, 14:5872-5884.
71. Zhang X., Lan W., Ems-McClung S.C., Stukenberg P.T., Walczak C.E. Aurora B phosphorylates multiple sites on mitotic centromere-associated kinesin to spatially and temporally regulate its function. Mol. Biol. Cell 2007, 18:3264-3276.