Cytoskeletal dynamics in caenorhabditis elegans axon regeneration

Annual Review of Cell and Developmental Biology

Volumn 29, Issue , 2013, Pages 271-297

  Chisholm, Andrew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

axotomy; DLK pathway; dynamic instability; growth cone; microtubule; neurofilament

Indexed keywords

LEUCINE ZIPPER PROTEIN; PROTEIN KINASE;

ACTIN FILAMENT; AXONAL INJURY; CAENORHABDITIS ELEGANS; CYTOSKELETON; GROWTH CONE; MICROTUBULE; NERVE FIBER REGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; CYTOLOGY; NERVE FIBER; PHYSIOLOGY; REGENERATION;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CYTOSKELETON; MICROTUBULES; REGENERATION;

EID: 84885769486     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-101512-122311     Document Type: Review

References (150)

1. Adler CE, Fetter RD, Bargmann CI. 2006. UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat. Neurosci. 9:511-18
2. Ahmad FJ, Joshi HC, Centonze VE, Baas PW. 1994. Inhibition of microtubule nucleation at the neuronal centrosome compromises axon growth. Neuron 12:271-80
3. Akhmanova A, Steinmetz MO. 2008. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9:309-22
4. Applegate KT, Besson S,Matov A, Bagonis MH, Jaqaman K, Danuser G. 2011. plus Tip Tracker: quantitative image analysis software for the measurement of microtubule dynamics. J. Struct. Biol. 176:168-84
5. Arimoto M, Koushika SP, Choudhary BC, Li C, Matsumoto K, Hisamoto N. Functions as an adaptor to link kinesin-1 with cytoplasmic dynein. J. Neurosci. 31:2216-24
6. Baas PW, Deitch JS, Black MM, Banker GA. 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA 85:8335-39
7. Baas PW, Falnikar A. 2012. Re-evaluation of the neuronal centrosome as a generator of microtubules for axons and dendrites. In The Centrosome, ed. H Schatten, pp. 309-26. New York: Humana
8. Bareyre FM, Garzorz N, Lang C, Misgeld T, Büning H, Kerschensteiner M. 2011. In vivo imaging reveals a phase-specific role of STAT3 during central and peripheral nervous system axon regeneration. Proc. Natl. Acad. Sci. USA 108:6282-87
9. Bieling P, Laan L, Schek H,Munteanu EL, Sandblad L, et al. 2007. Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450:1100-5
10. Bocquet A, Berges R, Frank R, Robert P, Peterson AC,Eyer J. 2009. Neurofilaments bind tubulin andmodulate its polymerization. J. Neurosci. 29:11043-54
11. Bounoutas A, Kratz J, Emtage L, Ma C, Nguyen KC, Chalfie M. 2011. Microtubule depolymerization in Caenorhabditis elegans touch receptor neurons reduces gene expression through a p38 MAPK pathway. Proc. Natl. Acad. Sci. USA 108:3982-87
12. Bounoutas A, O?Hagan R, Chalfie M. 2009. The multipurpose 15-protofilament microtubules in C. elegans have specific roles in mechanosensation. Curr. Biol. 19:1362-67
13. Bradke F, Fawcett JW, Spira ME. 2012. Assembly of a new growth cone after axotomy: the precursor to axon regeneration. Nat. Rev. Neurosci. 13:183-93
14. Buck KB,Zheng JQ. 2002. Growth cone turning induced by direct local modification ofmicrotubule dynamics. J. Neurosci. 22:9358-67
15. Burnette DT, Ji L, Schaefer AW, Medeiros NA, Danuser G, Forscher P. 2008. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell 15:163-69
16. Cassimeris L, Pryer NK, Salmon ED. 1988. Real-time observations of microtubule dynamic instability in living cells. J. Cell Biol. 107:2223-31
17. Cassimeris LU, Walker RA, Pryer NK, Salmon ED. 1987. Dynamic instability of microtubules. Bio Essays 7:149-54
18. Chalfie M, Thomson JN. 1979. Organization of neuronalmicrotubules in the nematode Caenorhabditis elegans. J. Cell Biol. 82:278-89
19. Chalfie M, Thomson JN. 1982. Structural and functional diversity in the neuronalmicrotubules of Caenorhabditis elegans. J. Cell Biol. 93:15-23
20. Chen L, Chisholm AD. 2011. Axon regeneration mechanisms: insights from C. elegans. Trends Cell Biol. 21:577-84
21. Chen L, Stone MC, Tao J, Rolls MM. 2012. Axon injury and stress trigger a microtubule-based neuroprotective pathway. Proc. Natl. Acad. Sci. USA 109:11842-47
22. Chen L, Wang Z, Ghosh-Roy A, Hubert T, Yan D, et al. 2011. Axon regeneration pathways identified by systematic genetic screening in C. elegans. Neuron 71:1043-57
23. Chen ZL, Yu WM, Strickland S. 2007. Peripheral regeneration. Annu. Rev. Neurosci. 30:209-33
24. Cho Y, Cavalli V. 2012. HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J. 31:3063-78
25. Conde C, Cáceres A. 2009. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10:319-32
26. Cueva JG, Hsin J, Huang KC, Goodman MB. 2012. Posttranslational acetylation of a-tubulin constrains protofilament number in native microtubules. Curr. Biol. 22:1066-74
27. Dent EW, Gupton SL, Gertler FB. 2011. The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3:a001800
28. Diamantopoulos GS, Perez F, Goodson HV, Batelier G,Melki R, et al. 1999. Dynamic localization of CLIP-170 to microtubule plus ends is coupled to microtubule assembly. J. Cell Biol. 144:99-112
29. El Bejjani R, Hammarlund M. 2012. Neural regeneration in Caenorhabditis elegans. Annu. Rev. Genet. 46:499-513
30. Erez H, Malkinson G, Prager-Khoutorsky M, De Zeeuw CI, Hoogenraad CC, Spira ME. 2007. Formation of microtubule-based traps controls the sorting and concentration of vesicles to restricted sites of regenerating neurons after axotomy. J. Cell Biol. 176:497-507
31. Erturk A, Hellal F, Enes J, Bradke F. 2007. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J. Neurosci. 27:9169-80
32. Falnikar A, Baas PW. 2009. Critical roles for microtubules in axonal development and disease. Cell Biol. Axon 48:47-64
33. Fang Y, Bonini NM. 2012. Axon degeneration and regeneration: insights from Drosophila models of nerve injury. Annu. Rev. Cell Dev. Biol. 28:575-97
34. Feldman JL, Priess JR. 2012. A role for the centrosome and PAR-3 in the hand-off of MTOC function during epithelial polarization. Curr. Biol. 22:575-82
35. Feltrin D, Fusco L, Witte H, Moretti F, Martin K, et al. 2012. Growth coneMKK7mRNAtargeting regulates MAP1b-dependent microtubule bundling to control neurite elongation. PLoS Biol. 10:e1001439
36. Filbin MT. 2003. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4:703-13
37. Franco M, Peters PJ, Boretto J, Van Donselaar E, Neri A, et al. 1999. EFA6, a sec7 domain-containing exchange factor for ARF6, coordinates membrane recycling and actin cytoskeleton organization. EMBO J. 18:1480-91
38. Frey D, Laux T, Xu L, Schneider C, Caroni P. 2000. Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J. Cell Biol. 149:1443-54
39. Gabel CV, Antoine F, Chuang CF, Samuel AD, Chang C. 2008. Distinct cellular and molecular mechanisms mediate initial axon development and adult-stage axon regeneration in C. elegans. Development 135:1129-36
40. Gardner MK, Zanic M, Howard J. 2013. Microtubule catastrophe and rescue. Curr. Opin. Cell Biol. 25:14-22
41. Garnham CP, Roll-Mecak A. 2012. The chemical complexity of cellular microtubules: tubulin posttranslationalmodification enzymes and their roles in tuningmicrotubule functions. Cytoskeleton 69:442-63
42. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev. Cell 23:716-28
43. Ghosh-Roy A, Wu Z, Goncharov A, Jin Y, Chisholm AD. 2010. Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J. Neurosci. 30:3175-83
44. Gitler D, Spira ME. 1998. Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 20:1123-35
45. Goedert M, Baur CP, Ahringer J, Jakes R, HasegawaM, et al. 1996. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J. Cell Sci. 109:2661-72
46. Goodwin PR, Sasaki JM, Juo P. 2012. Cyclin-dependent kinase 5 regulates the polarized trafficking of neuropeptide-containing dense-core vesicles in Caenorhabditis elegans motor neurons. J. Neurosci. 32:8158-72
47. Goodwin SS, Vale RD. 2010. Patronin regulates the microtubule network by protecting microtubule minus ends. Cell 143:263-74
48. Halpain S, Dehmelt L. 2006. The MAP1 family of microtubule-associated proteins. Genome Biol. 7:224
49. Hammarlund M, Jorgensen EM, Bastiani MJ. 2007. Axons break in animals lacking ß-spectrin. J. Cell Biol. 176:269-75
50. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M. 2009. Axon regeneration requires a conserved MAP kinase pathway. Science 323:802-6
51. Harris A, Morgan JI, Pecot M, Soumare A, Osborne A, Soares HD. 2000. Regenerating motor neurons express Nna1, a novel ATP/GTP-binding protein related to zinc carboxypeptidases. Mol. Cell. Neurosci. 16:578-96
52. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, et al. 2011. Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331:928-31
53. Hendricks M, Jesuthasan S. 2009. PHR regulates growth cone pausing at intermediate targets through microtubule disassembly. J. Neurosci. 29:6593-98
54. Hirai S, Banba Y, Satake T, Ohno S. 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. 31:6468-80
55. Hoffman PN, Cleveland DW. 1988. Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: induction of a specific ß-tubulin isotype. Proc. Natl. Acad. Sci. USA 85:4530-33
56. Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL. 1987. Neurofilament gene expression: a major determinant of axonal caliber. Proc. Natl. Acad. Sci. USA 84:3472-76
57. Hoffman PN, Lasek RJ. 1980. Axonal transport of the cytoskeleton in regenerating motor neurons: constancy and change. Brain Res. 202:317-33
58. Hoffman PN, Pollock SC, Striph GG. 1993. Altered gene expression after optic nerve transection: reduced neurofilament expression as a general response to axonal injury. Exp. Neurol. 119:32-36
59. Homma N, Takei Y, Tanaka Y, Nakata T, Terada S, et al. 2003. Kinesin superfamily protein 2A (KIF2A) functions in suppression of collateral branch extension. Cell 114:229-39
60. Hoogenraad CC, Bradke F. 2009. Control of neuronal polarity and plasticity-a renaissance for microtubules? Trends Cell Biol. 19:669-76
61. Horiuchi D, Collins CA, Bhat P, Barkus RV, Diantonio A, Saxton WM. 2007. Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr. Biol. 17:1313-17
62. Hur E-M, Saijilafu, Zhou FQ. 2011a. Growing the growth cone: remodeling the cytoskeleton to promote axon regeneration. Trends Neurosci. 35:164-74
63. Hur E-M, Yang IH, Kim D-H, Byun J, Saijilafu, et al. 2011b. Engineering neuronal growth cones to promote axon regeneration over inhibitory molecules. Proc. Natl. Acad. Sci. USA 108:5057-62
64. Itoh A, Horiuchi M, Bannerman P, Pleasure D, Itoh T. 2009. Impaired regenerative response of primary sensory neurons in ZPK/DLK gene-trap mice. Biochem. Biophys. Res. Commun. 383:258-62
65. Janke C, Bulinski JC. 2011. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12:773-86
66. Janke C, Kneussel M. 2010. Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 33:362-72
67. Kabir N, Schaefer AW, Nakhost A, Sossin WS, Forscher P. 2001. Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152:1033-44
68. Kapitein LC, Hoogenraad CC. 2011. Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol. Cell Neurosci. 46:9-20
69. Karabinos A, Schmidt H, Harborth J, Schnabel R, Weber K. 2001. Essential roles for four cytoplasmic intermediate filament proteins in Caenorhabditis elegans development. Proc. Natl. Acad. Sci. USA 98:7863-68
70. Karabinos A, Schunemann J, Weber K. 2004. Most genes encoding cytoplasmic intermediate filament (IF) proteins of the nematode Caenorhabditis elegans are required in late embryogenesis. Eur. J. Cell Biol. 83:457-68
71. Kimura Y, Kurabe N, Ikegami K, Tsutsumi K, Konishi Y, et al. 2010. Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J. Biol. Chem. 285:22936-41
72. Kirszenblat L, Neumann B, Coakley S, Hilliard MA. 2013. A dominant mutation in mec-7/ß-tubulin affects axon development and regeneration in Caenorhabditis elegans neurons. Mol. Biol. Cell 24:285-96
73. Knobel KM, Jorgensen EM, Bastiani MJ. 1999. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126:4489-98
74. Kuijpers M, Hoogenraad CC. 2011. Centrosomes, microtubules and neuronal development. Mol. CellNeurosci. 48:349-58
75. Lacroix B, Van Dijk J, Gold ND, Guizetti J, Aldrian-Herrada G, et al. 2010. Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J. Cell Biol. 189:945-54
76. Laskowski CJ, Bradke F. 2012. In vivo imaging: a dynamic imaging approach to study spinal cord regeneration. Exp. Neurol. 242:11-17
77. Lewcock JW, Genoud N, Lettieri K, Pfaff SL. 2007. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56:604-20
78. Li C, Hisamoto N, Nix P, Kanao S, Mizuno T, et al. 2012. The growth factor SVH-1 regulates axon regeneration in C. elegans via the JNK MAPK cascade. Nat. Neurosci. 15:551-57
79. Liu K, Tedeschi A, Park KK, He Z. 2011. Neuronal intrinsic mechanisms of axon regeneration. Annu. Rev. Neurosci. 34:131-52
80. Maniar TA, Kaplan M, Wang GJ, Shen K, Wei L, et al. 2012. UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat. Neurosci. 15:48-56
81. Meng W, Mushika Y, Ichii T, Takeichi M. 2008. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135:948-59
82. Mitchison T, Kirschner M. 1984. Dynamic instability of microtubule growth. Nature 312:237-42
83. Motegi F, Velarde NV, Piano F, Sugimoto A. 2006.Twophases of astralmicrotubule activity during cytokinesis in C. elegans embryos. Dev. Cell 10:509-20
84. Nadeau S, Hein P, Fernandes KJL, Peterson AC, Miller FD. 2005. A transcriptional role for C/EBP ßin the neuronal response to axonal injury. Mol. Cell. Neurosci. 29:525-35
85. Nakata K, Abrams B, Grill B, Goncharov A, Huang X, et al. 2005. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407-20
86. Nawabi H, Zukor K, He Z. 2012. No simpler than mammals: axon and dendrite regeneration in Drosophila. Genes Dev. 26:1509-14
87. Nechipurenko IV, Broihier HT. 2012. Fox O limits microtubule stability and is itself negatively regulated by microtubule disruption. J. Cell Biol. 196:345-62
88. Neumann B, Nguyen KC, Hall DH, Ben-Yakar A, Hilliard MA. 2011. Axonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons. Dev. Dyn. 240:1365-72
89. Ng DC, Zhao TT, Yeap YY, Ngoei KR, Bogoyevitch MA. 2010. c-Jun N-terminal kinase phosphorylation of stathmin confers protection against cellular stress. J. Biol. Chem. 285:29001-13
90. Nguyen MM, Stone MC, Rolls MM. 2011. Microtubules are organized independently of the centrosome in Drosophila neurons. Neural Dev. 6:38
91. Nix P, Hisamoto N, Matsumoto K, Bastiani M. 2011. Axon regeneration requires coordinate activation of p38 and JNK MAPK pathways. Proc. Natl. Acad. Sci. USA 108:10738-43
92. O?Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KCQ, et al. 2011. The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr. Biol. 21:1685-94
93. O?Rourke SM, Christensen SN, Bowerman B. 2010. Caenorhabditis elegans EFA-6 limits microtubule growth at the cell cortex. Nat. Cell Biol. 12:1235-41
94. Oblinger MM, Lasek RJ. 1988. Axotomy-induced alterations in the synthesis and transport of neurofilaments and microtubules in dorsal root ganglion cells. J. Neurosci. 8:1747-58
95. Ori-McKenney KM, Jan LY, Jan YN. 2012. Golgi outposts shape dendritemorphology by functioning as sites of acentrosomal microtubule nucleation in neurons. Neuron 76:921-30
96. Ou CY, Poon VY, Maeder CI, Watanabe S, Lehrman EK, et al. 2010. Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components. Cell 141:846-58
97. Ou CY, Shen K. 2011. Neuronal polarity in C. elegans. Dev. Neurobiol. 71:554-66
98. Paturle-Lafanech́ere L, Eddé B, Denoulet P, Van Dorsselaer A,Mazarguil H, et al Characterization of a major brain tubulin variant which cannot be tyrosinated Biochemistry 30 10523-28
99. Paturle-Lafanech́ere L, Manier M, Trigault N, Pirollet F, Mazarguil H, Job D. 1994. Accumulation of delta 2-tubulin, a major tubulin variant that cannot be tyrosinated, in neuronal tissues and in stablemicrotubule assemblies. J. Cell Sci. 107:1529-43
100. Perez F, Diamantopoulos GS, Stalder R, Kreis TE. 1999. CLIP-170 highlights growing microtubule ends in vivo. Cell 96:517-27
101. Peris L, Wagenbach M, Lafanech́ere L, Brocard J, Moore AT, et al. 2009. Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. Cell Biol. 185:1159-66
102. Pinan-Lucarre B, Gabel CV, Reina CP, Hulme SE, Shevkoplyas SS, et al. 2012. The core apoptotic executioner proteins CED-3 and CED-4 promote initiation of neuronal regeneration in Caenorhabditis elegans. PLoS Biol. 10:e1001331
103. Polleux F, Snider W. 2010. Initiating and growing an axon. Cold Spring Harb. Perspect. Biol. 2:a001925
104. Qiu J, Cafferty WB, McMahon SB, Thompson SW. 2005. Conditioning injury-induced spinal axon regeneration requires signal transducer and activator of transcription 3 activation. J. Neurosci. 25:1645-53
105. Ramón y Cajal S. 1991. Cajal.s Degeneration and Regeneration of the Nervous System, ed. J DeFelipe, EG Jones, transl. RM May. New York: Oxford Univ. Press
106. Roll-Mecak A, McNally FJ. 2010. Microtubule-severing enzymes. Curr. Opin. Cell Biol. 22:96-103
107. Roll-Mecak A, Vale RD. 2006. Making more microtubules by severing: A common theme of noncentrosomal microtubule arrays? J. Cell Biol. 175:849-51
108. Rolls MM, Satoh D, Clyne PJ, Henner AL, Uemura T, Doe CQ. 2007. Polarity and intracellular compartmentalization of Drosophila neurons. Neural Dev. 2:7
109. Sahly I, Khoutorsky A, Erez H, Prager-Khoutorsky M, Spira ME. 2006. On-line confocal imaging of the events leading to structural dedifferentiation of an axonal segment into a growth cone after axotomy. J. Comp. Neurol. 494:705-20
110. Samara C, Rohde CB, Gilleland CL, Norton S, Haggarty SJ, YanikMF. 2010. Large-scale in vivo femtosecond laser neurosurgery screen reveals small-molecule enhancer of regeneration. Proc. Natl. Acad. Sci. USA 107:18342-47
111. Savage C, Hamelin M, Culotti JG, Coulson A, Albertson DG, Chalfie M. 1989. mec-7 is a ß-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 3:870-81
112. Scholey JM. 2008. Intraflagellar transportmotors in cilia: moving along the cell's antenna. J. Cell Biol. 180:23-29
113. Selvaraj BT, Frank N, Bender FLP, Asan E, Sendtner M. 2012. Local axonal function of STAT3 rescues axon degeneration in the pmn model of motoneuron disease. J. Cell Biol. 199:437-51
114. Sengottuvel V, Leibinger M, Pfreimer M, Andreadaki A, Fischer D. 2011. Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 31:2688-99
115. Shi S-H, Cheng T, Jan LY, Jan YN. 2004. APC and GSK-3ßare involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14:2025-32
116. Shin JE, Cho Y, Beirowski B, Milbrandt J,Cavalli V, Di Antonio A. 2012. Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration. Neuron 74:1015-22
117. Song Y, Ori-McKenney KM, Zheng Y, Han C, Jan LY, Jan YN. 2012. Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and micro RNA bantam. Genes Dev. 26:1612-25
118. Spira ME, Oren R, Dormann A, Gitler D. 2003. Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons. J. Comp. Neurol. 457:293-312
119. Srayko M, Quintin S, Schwager A, Hyman AA. 2003. Caenorhabditis elegans TAC-1 and ZYG-9 form a complex that is essential for long astral and spindle microtubules. Curr. Biol. 13:1506-11
120. Stepanova T, Slemmer J,Hoogenraad CC, Lansbergen G, DortlandB, et al. 2003. Visualization ofmicrotubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23:2655-64
121. Stepanova T, Smal I, Van Haren J, Akinci U, Liu Z, et al. 2010. History-dependent catastrophes regulate axonal microtubule behavior. Curr. Biol. 20:1023-28
122. Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, et al. 2010. Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704-7
123. Stone MC, Nguyen MM, Tao J, Allender DL, Rolls MM.2010. Global up-regulation ofmicrotubule dynamics and polarity reversal during regeneration of an axon from a dendrite. Mol. Biol. Cell 21:767-77
124. Stone MC, Rao K, Gheres KW, Kim S, Tao J, et al. 2012. Normal spastin gene dosage is specifically required for axon regeneration. Cell Rep. 2:1340-50
125. Stone MC, Roegiers F, Rolls MM. 2008. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol. Biol. Cell 19:4122-29
126. Suter DM, Miller KE. 2011. The emerging role of forces in axonal elongation. Prog. Neurobiol. 94:91-101
127. Szaro BG, Strong MJ. 2010. Post-transcriptional control of neurofilaments: new roles in development, regeneration and neurodegenerative disease. Trends Neurosci. 33:27-37
128. Tanaka EM, Kirschner MW. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J. Cell Biol. 115:345-63
129. Tararuk T, Östman N, Li W, BjÖ rkblom B, Padzik A, et al. 2006. JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J. Cell Biol. 173:265-77
130. Tedeschi A. 2011. Tuning the orchestra: transcriptional pathways controlling axon regeneration. Front. Mol. Neurosci. 4:60
131. Topalidou I, Keller C, Kalebic N, Nguyen KCQ, Somhegyi H, et al. 2012. Genetically separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization. Curr. Biol. 22:1057-65
132. Tuszynski MH, Steward O. 2012. Concepts and methods for the study of axonal regeneration in the CNS. Neuron 74:777-91
133. Walker RA, O?Brien ET, Pryer NK, Soboeiro MF, Voter WA, et al. 1988. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107:1437-48
134. Wang Z, Jin Y. 2011. Genetic dissection of axon regeneration. Curr. Opin. Neurobiol. 21:189-96
135. Watkins TA, Wang B, Huntwork-Rodriguez S, Yang J, Jiang Z, et al. 2013. DLK initiates a transcriptional program that couples apoptotic and regenerative responses to axonal injury. Proc. Natl. Acad. Sci. USA 110:4039-44
136. Webster DR, Gundersen GG, Bulinski JC, Borisy GG. 1987. Differential turnover of tyrosinated and detyrosinated microtubules. Proc. Natl. Acad. Sci. USA 84:9040-44
137. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. B Biol. Sci. 314:1-340
138. Witte H, Neukirchen D, Bradke F. 2008. Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180:619-32
139. Wu Z, Ghosh-Roy A, Yanik MF, Zhang JZ, Jin Y, Chisholm AD. 2007. Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching. Proc. Natl. Acad. Sci. USA 104:15132-37
140. Xiong X, Wang X, Ewanek R, Bhat P, Di Antonio A, Collins CA. 2010. Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J. Cell Biol. 191:211-23
141. Xu K, Zhong G, Zhuang X. 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339:452-56
142. Yan D, Jin Y. 2012. Regulation of DLK-1 kinase activity by calcium-mediated dissociation from an inhibitory isoform. Neuron 76:534-48
143. Yan D,Wu Z, Chisholm AD, Jin Y. 2009. The DLK-1 kinase promotes m RNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005-18
144. Yanik MF, Cinar H, Cinar HN, Chisholm AD, Jin Y, Ben-Yakar A. 2004. Neurosurgery: functional regeneration after laser axotomy. Nature 432:822
145. Yu W, Ahmad FJ, Baas PW. 1994. Microtubule fragmentation and partitioning in the axon during collateral branch formation. J. Neurosci. 14:5872-84
146. Yu W, Centonze VE, Ahmad FJ, Baas PW. 1993. Microtubule nucleation and release from the neuronal centrosome. J. Cell Biol. 122:349-59
147. Yuan A, Rao MV, Veeranna, Nixon RA. 2012. Neurofilaments at a glance. J. Cell Sci. 125:3257-63
148. Zheng B, Lee JK, Xie F. 2006. Genetic mouse models for studying inhibitors of spinal axon regeneration. Trends Neurosci. 29:640-46
149. Ziv NE, Spira ME. 1993. Spatiotemporal distribution of Ca2+ following axotomy and throughout the recovery process of cultured Aplysia neurons. Eur. J. Neurosci. 5:657-68
150. Ziv NE, Spira ME. 1997. Localized and transient elevations of intracellular Ca2+ induce the dedifferentiation of axonal segments into growth cones. J. Neurosci. 17:3568-79