The role of local protein synthesis and degradation in axon regeneration

Experimental Neurology

Volumn 223, Issue 1, 2010, Pages 28-37

  Gumy, Laura F ^a   Tan, Chin Lik ^a   Fawcett, James W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Axon regeneration; Growth cone formation; Local degradation; Local protein synthesis

Indexed keywords

ANISOMYCIN; BETA ACTIN; BETA TUBULIN; CALCIUM; CALPAIN; CYCLOHEXIMIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUROTROPHIN; PROTEASOME; RIBOSOME RNA; TRANSFER RNA; UBIQUITIN;

AUTOPHAGY; AXONAL INJURY; CENTRAL NERVOUS SYSTEM; CYTOSKELETON; GROWTH CONE; HUMAN; NERVE CELL CULTURE; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SPINAL GANGLION; UBIQUITINATION;

ANIMALS; AUTOPHAGY; AXONS; CALCIUM; CALPAIN; GROWTH CONES; NERVE REGENERATION; NERVE TISSUE PROTEINS; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; UBIQUITIN;

EID: 77950863408     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.06.004     Document Type: Review

References (118)

1. Abrams T.W., Yovell Y., Onyike C.U., Cohen J.E., Jarrard H.E. Analysis of sequence-dependent interactions between transient calcium and transmitter stimuli in activating adenylyl cyclase in Aplysia: possible contribution to CS-US sequence requirement during conditioning. Learn Mem. 1998, 4:496-509.
2. Alvarez J., Giuditta A., Koenig E. Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol. 2000, 62:1-62.
3. Aschrafi A., Schwechter A.D., Mameza M.G., Natera-Naranjo O., Gioio A.E., Kaplan B.B. MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J. Neurosci. 2008, 28:12581-12590.
4. Aunis D., Bader M.F. The cytoskeleton as a barrier to exocytosis in secretory cells. J. Exp. Biol. 1988, 139:253-266.
5. Bamburg J.R., McGough A., Ono S. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol. 1999, 9:364-370.
6. Banik N.L., Matzelle D.C., Gantt-Wilford G., Osborne A., Hogan E.L. Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res. 1997, 752:301-306.
7. Bassell G.J., Kelic S. Binding proteins for mRNA localization and local translation, and their dysfunction in genetic neurological disease. Curr. Opin. Neurobiol. 2004, 14:574-581.
8. Bassell G.J., Zhang H., Byrd A.L., Femino A.M., Singer R.H., Taneja K.L., Lifshitz L.M., Herman I.M., Kosik K.S. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 1998, 18:251-265.
9. Benbassat D., Spira M.E. Survival of isolated axonal segments in culture: morphological, ultrastructural, and physiological analysis. Exp. Neurol. 1993, 122:295-310.
10. Bennett V., Baines A.J. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 2001, 81:1353-1392.
11. Campbell D.S., Holt C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 2001, 32:1013-1026.
12. Campbell D.S., Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 2003, 37:939-952.
13. Chakraborty G., Ingoglia N.A. N-terminal arginylation and ubiquitin-mediated proteolysis in nerve regeneration. Brain Res. Bull. 1993, 30:439-445.
14. Chierzi S., Ratto G.M., Verma P., Fawcett J.W. The ability of axons to regenerate their growth cones depends on axonal type and age, and is regulated by calcium, cAMP and ERK. Eur. J. Neurosci. 2005, 21:2051-2062.
15. Chun J.T., Gioio A.E., Crispino M., Giuditta A., Kaplan B.B. Characterization of squid enolase mRNA: sequence analysis, tissue distribution, and axonal localization. Neurochem. Res. 1995, 20:923-930.
16. Chun J.T., Gioio A.E., Crispino M., Eyman M., Giuditta A., Kaplan B.B. Molecular cloning and characterization of a novel mRNA present in the squid giant axon. J. Neurosci. Res. 1997, 49:144-153.
17. Court F.A., Hendriks W.T., Macgillavry H.D., Alvarez J., van Minnen J. Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J. Neurosci. 2008, 28:11024-11029.
18. Cox L.J., Hengst U., Gurskaya N.G., Lukyanov K.A., Jaffrey S.R. Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat. Cell Biol. 2008, 10:149-159.
19. Cubells J.F., Rayport S., Rajendran G., Sulzer D. Methamphetamine neurotoxicity involves vacuolation of endocytic organelles and dopamine-dependent intracellular oxidative stress. J. Neurosci. 1994, 14:2260-2271.
20. Cuervo A.M. Autophagy: in sickness and in health. Trends Cell Biol. 2004, 14(2):70-77.
21. Du T.G., Schmid M., Jansen R.P. Why cells move messages: the biological functions of mRNA localization. Semin. Cell Dev. Biol. 2007, 18:171-177.
22. Edbladh M., Tonge D., Golding J., Ekstrom A.R., Edstrom A. Early regeneration in vitro of adult mouse sciatic axons is dependent on local protein synthesis but may not involve neurotrophins. Neurosci. Lett. 1994, 168:37-40.
23. Eddleman C.S., Bittner G.D., Fishman H.M. Barrier permeability at cut axonal ends progressively decreases until an ionic seal is formed. Biophys. J. 2000, 79:1883-1890.
24. Eng H., Lund K., Campenot R.B. Synthesis of beta-tubulin, actin, and other proteins in axons of sympathetic neurons in compartmented cultures. J. Neurosci. 1999, 19:1-9.
25. Ferber S., Ciechanover A. Role of arginine-tRNA in protein degradation by the ubiquitin pathway. Nature 1987, 326:808-811.
26. Frankel R.D., Koenig E. Identification of locally synthesized proteins in proximal stump axons of the neurotomized hypoglossal nerve. Brain Res. 1978, 141:67-76.
27. Friede R.L., Bischhausen R. The fine structure of stumps of transected nerve fibers in subserial sections. J. Neurol. Sci. 1980, 44:181-203.
28. Gabso M., Neher E., Spira M.E. Low mobility of the Ca2+ buffers in axons of cultured Aplysia neurons. Neuron 1997, 18:473-481.
29. Gaete J., Kameid G., Alvarez J. Regenerating axons of the rat require a local source of proteins. Neurosci. Lett. 1998, 251:197-200.
30. Ghosh M., Song X., Mouneimne G., Sidani M., Lawrence D.S., Condeelis J.S. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004, 304:743-746.
31. Gioio A.E., Lavina Z.S., Jurkovicova D., Zhang H., Eyman M., Giuditta A., Kaplan B.B. Nerve terminals of squid photoreceptor neurons contain a heterogeneous population of mRNAs and translate a transfected reporter mRNA. Eur. J. Neurosci. 2004, 20:865-872.
32. Gitler D., Spira M.E. Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 1998, 20:1123-1135.
33. Giuditta A., Menichini E., Perrone Capano C., Langella M., Martin R., Castigli E., Kaplan B.B. Active polysomes in the axoplasm of the squid giant axon. J. Neurosci. Res. 1991, 28:18-28.
34. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82:373-428.
35. Godell C.M., Smyers M.E., Eddleman C.S., Ballinger M.L., Fishman H.M., Bittner G.D. Calpain activity promotes the sealing of severed giant axons. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4751-4756.
36. Hanz S., Perlson E., Willis D., Zheng J.Q., Massarwa R., Huerta J.J., Koltzenburg M., Kohler M., van-Minnen J., Twiss J.L., Fainzilber M. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 2003, 40:1095-1104.
37. Hedge A.N. Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog. Neurobiol. 2004, 73:311-357.
38. Hengst U., Cox L.J., Macosko E.Z., Jaffrey S.R. Functional and selective RNA interference in developing axons and growth cones. J. Neurosci. 2006, 26:5727-5732.
39. Hollenbeck P.J. Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 1993, 121:305-315.
40. Howard M.J., David G., Barrett J.N. Resealing of transected myelinated mammalian axons in vivo: evidence for involvement of calpain. Neuroscience 1999, 93:807-815.
41. Jack D.L., Chakraborty G., Ingoglia N.A. Ubiquitin is associated with aggregates of arginine modified proteins in injured nerves. Neuroreport 1992, 3:47-50.
42. Johnston J.A., Madura K. Rings, chains and ladders: ubiquitin goes to work in the neuron. Prog. Neurobiol. 2004, 73:227-257.
43. Kavakebi P., Hausott B., Tomasino A., Ingorokva S., Klimaschewski L. The N-end rule ubiquitin-conjugating enzyme, HR6B, is up-regulated by nerve growth factor and required for neurite outgrowth. Mol. Cell Neurosci. 2005, 29:559-568.
44. Kindler S., Wang H., Richter D., Tiedge H. RNA transport and local control of translation. Annu. Rev. Cell Dev. Biol. 2005, 21:223-245.
45. Klimaschewski L., Hausott B., Ingorokva S., Pfaller K. Constitutively expressed catalytic proteasomal subunits are up-regulated during neuronal differentiation and required for axon initiation, elongation and maintenance. J. Neurochem. 2006, 96:1708-1717.
46. Koenig E. Synthetic mechanisms in the axon. I. Local axonal synthesis of acetylcholinesterase. J. Neurochem. 1965, 12:343-355.
47. Koenig E. Synthetic mechanisms in the axon. III. Stimulation of acetylcholinesterase synthesis by actinomycin-D in the hypoglossal nerve. J. Neurochem. 1967, 14:429-435.
48. Koenig E. Cycloheximide-sensitive [35S]methionine labeling of proteins in goldfish retinal ganglion cell axons in vitro. Brain Res. 1989, 481:119-123.
49. Koenig E., Adams P. Local protein synthesizing activity in axonal fields regenerating in vitro. J. Neurochem. 1982, 39:386-400.
50. Koenig E., Martin R. Cortical plaque-like structures identify ribosome-containing domains in the Mauthner cell axon. J. Neurosci. 1996, 16:1400-1411.
51. Koenig E., Martin R., Titmus M., Sotelo-Silveira JR. Cryptic peripheral ribosomal domains distributed intermittently along mammalian myelinated axons. J. Neurosci. 2000, 20:8390-8400.
52. Komatsu M., Wang Q.J., Holstein G.R., Friedrich V.L., Iwata J., Kominami E., Chait B.T., Tanaka K., Yue Z. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14489-14494.
53. Kosik K.S. The neuronal microRNA system. Nat. Rev. Neurosci. 2006, 7:911-920.
54. Kun A., Otero L., Sotelo-Silveira J.R., Sotelo J.R. Ribosomal distributions in axons of mammalian myelinated fibers. J. Neurosci. Res 2007, 85:2087-2098.
55. Larsen K.E., Sulzer D. Autophagy in neurons: a review. Histol. Histopathol. 2002, 17:897-908.
56. Laser H., Mack T.G., Wagner D., Coleman M.P. Proteasome inhibition arrests neurite outgrowth and causes "dying-back" degeneration in primary culture. J. Neurosci. Res. 2003, 74:906-916.
57. Lerner E.A., Lerner M.R., Janeway C.A., Steitz J.A.. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:2737-2741.
58. 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.
59. Mandolesi G., Madeddu F., Bozzi Y., Maffei L., Ratto G.M. Acute physiological response of mammalian central neurons to axotomy: ionic regulation and electrical activity. FASEB J. 2004, 18:1934-1936.
60. Matthews M.R. An ultrastructural study of axonal changes following constriction of postganglionic branches of the superior cervical ganglion in the rat. Philos. Trans. R Soc. Lond., B Biol. Sci. 1973, 264:479-505.
61. Matthews M.R., Raisman G. A light and electron microscopic study of the cellular response to axonal injury in the superior cervical ganglion of the rat. Proc. R Soc. Lond., B Biol. Sci. 1972, 181:43-79.
62. Mingorance-Le Meur A., O'Connor T.P. Neurite consolidation is an active process requiring constant repression of protrusive activity. EMBO J. 2008, 28:248-260.
63. Murashov A.K., Chintalgattu V., Islamov R.R., Lever T.E., Pak E.S., Sierpinski P.L., Katwa L.C., Van Scott M.R. RNAi pathway is functional in peripheral nerve axons. FASEB J. 2007, 21:656-670.
64. Murphey R.K., Godenschwege T.A. New roles for ubiquitin in the assembly and function of neuronal circuits. Neuron 2002, 36:5-8.
65. Olink-Coux M., Hollenbeck P.J. Localization and active transport of mRNA in axons of sympathetic neurons in culture. J. Neurosci. 1996, 16:1346-1358.
66. Onyike C.U., Lin A.H., Abrams T.W. Persistence of the interaction of calmodulin with adenylyl cyclase: implications for intergration of transient calcium stimuli. J. Neurochem. 1998, 71:1298-1306.
67. Pan Y.A., Misgeld T., Lichtman J.W., Sanes J.R. Effects of neurotoxic and neuroprotective agents on peripheral nerve regeneration assayed by time-lapse imaging in vivo. J. Neurosci. 2003, 23:11479-11488.
68. Pannese E., Ledda M. Ribosomes in myelinated axons of the rabbit spinal ganglion neurons. J. Submicrosc. Cytol. Pathol. 1991, 23:33-38.
69. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
70. Perlson E., Hanz S., Ben-Yaakov K., Segal-Ruder Y., Seger R., Fainzilber M. Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 2005, 45:715-726.
71. Perlson E., Michaelevski I., Kowalsman N., Ben-Yaakov K., Shaked M., Seger R., Eisenstein M., Fainzilber M. Vimentin binding to phosphorylated Erk sterically hinders enzymatic dephosphorylation of the kinase. J. Mol. Biol. 2006, 364:938-944.
72. Piper M., Holt C. RNA translation in axons. Annu. Rev. Cell Dev. Biol. 2004, 20:505-523.
73. Reynolds A.J., Hendry I.A., Bartlett S.E. Anterograde and retrograde transport of active extracellular signal-related kinase 1 (ERK1) in the ligated rat sciatic nerve. Neuroscience 2001, 105:761-771.
74. Rishal I., Fainzilber M. Retrograde signaling in axonal regeneration. Exp. Neurol. 2010, 223:5-10.
75. Rubinsztein D.C., DiFiglia M., Heintz N., Nixon R.A., Qin Z.H., Ravikumar B., Stefanis L., Tolkovsky A. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 2005, 1:11-22.
76. Sahly I., Khoutorsky A., Erez H., Prager-Khoutorsky M., Spira M.E. On-line confocal imaging of the events leading to structural dedifferentiation of an axonal segment into a growth cone after axotomy. J. Comp. Neurol. 2006, 494:705-720.
77. Shi R., Asano T., Vining N.C., Blight A.R. Control of membrane sealing in injured mammalian spinal cord axons. J. Neurophysiol. 2000, 84:1763-1769.
78. Shyne-Athwal S., Riccio R.V., Chakraborty G., Ingoglia N.A. Protein modification by amino acid addition is increased in crushed sciatic but not optic nerves. Science 1986, 231:603-605.
79. Shyne-Athwal S., Chakraborty G., Gage E., Ingoglia N.A. Comparison of posttranslational protein modification by amino acid addition after crush injury to sciatic and optic nerves of rats. Exp. Neurol. 1988, 99:281-295.
80. Sossin W.S., DesGroseillers L. Intracellular trafficking of RNA in neurons. Traffic 2006, 7:1581-1589.
81. Sotelo J.R., Kun A., Benech J.C., Giuditta A., Morillas J., Benech C.R. Ribosomes and polyribosomes are present in the squid giant axon: an immunocytochemical study. Neuroscience 1999, 90:705-715.
82. Sotelo-Silveira J.R., Calliari A., Kun A., Koenig E., Sotelo J.R. RNA trafficking in axons. Traffic 2006, 7:508-515.
83. Speese S.D., Trotta N., Rodesch C.K., Aravamudan B., Broadie K. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 2003, 13:899-910.
84. Spira M.E., Benbassat D., Dormann A. Resealing of the proximal and distal cut ends of transected axons: electrophysiological and ultrastructural analysis. J. Neurobiol. 1993, 24:300-316.
85. Spira M.E., Dormann A., Ashery U., Gabso M., Gitler D., Benbassat D., Oren R., Ziv N.E. Use of Aplysia neurons for the study of cellular alterations and the resealing of transected axons in vitro. J. Neurosci. Methods 1996, 69:91-102.
86. Spira M.E., Oren R., Dormann A., Ilouz N., Lev S. Calcium, protease activation, and cytoskeleton remodeling underlie growth cone formation and neuronal regeneration. Cell Mol. Neurobiol. 2001, 21:591-604.
87. Spira M.E., Oren R., Dormann A., Gitler D. 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. 2003, 457:293-312.
88. Springer J.E., Azbill R.D., Kennedy S.E., George J., Geddes J.W. Rapid calpain I activation and cytoskeletal protein degradation following traumatic spinal cord injury: attenuation with riluzole pretreatment. J. Neurochem. 1997, 69:1592-1600.
89. Staal J.A., Dickson T.C., Chung R.S., Vickers J.C. Disruption of the ubiquitin proteasome system following axonal stretch injury accelerates progression to secondary axotomy. J. Neurotrauma 2009, 26:781-788.
90. Sung Y.J., Povelones M., Ambron R.T. RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J. Neurobiol. 2001, 47:67-79.
91. Taylor A.M., Berchtold N.C., Perreau V.M., Tu C.H., Li Jeon N., Cotman C.W. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 2009, 29:4697-4707.
92. Tobias G.S., Koenig E. Axonal protein synthesizing activity during the early outgrowth period following neurotomy. Exp. Neurol. 1975, 49:221-234.
93. Tobias G.S., Koenig E. Influence of nerve cell body and neurolemma cell on local axonal protein synthesis following neurotomy. Exp. Neurol. 1975, 49:235-245.
94. Tonge D., Chan K., Zhu N., Panjwani A., Arno M., Lynham S., Ward M., Snape A., Pizzey J. Enhancement of axonal regeneration by in vitro conditioning and its inhibition by cyclopentenone prostaglandins. J. Cell Sci. 2008, 121:2565-2577.
95. Tursun B., Schluter A., Peters M.A., Viehweger B., Ostendorff H.P., Soosairajah J., Drung A., Bossenz M., Johnsen S.A., Schweizer M., Bernard O., Bach I. The ubiquitin ligase Rnf6 regulates local LIM kinase 1 levels in axonal growth cones. Genes Dev. 2005, 19:2307-2319.
96. Twiss J.L., Smith D.S., Chang B., Shooter E.M. Translational control of ribosomal protein L4 mRNA is required for rapid neurite regeneration. Neurobiol. Dis. 2000, 7:416-428.
97. van Horck F.P., Weinl C., Holt C.E. Retinal axon guidance: novel mechanisms for steering. Curr. Opin. Neurobiol. 2004, 14:61-66.
98. van Tijn P., Hol E.M., van Leeuwen F.W., Fischer D.F. The neuronal ubiquitin-proteasome system: murine models and their neurological phenotype. Prog. Neurobiol. 2008, 85:176-193.
99. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., Fawcett J.W. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25:331-342.
100. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16426-16431.
101. Wang W., van Niekerk E., Willis D.E., Twiss J.L. RNA transport and localized protein synthesis in neurological disorders and neural repair. Dev. Neurobiol. 2007, 67:1166-1182.
102. Watts R.J., Hoopfer E.D., Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 2003, 38:871-875.
103. Willis D.E., Twiss J.L. The evolving roles of axonally synthesized proteins in regeneration. Curr. Opin. Neurobiol. 2006, 16:111-118.
104. Willis D., Li K.W., Zheng J.Q., Chang J.H., Smit A., Kelly T., Merianda T.T., Sylvester J., van Minnen J., Twiss J.L. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. J. Neurosci. 2005, 25:778-791.
105. Willis D.E., van Niekerk E.A., Sasaki Y., Mesngon M., Merianda T.T., Williams G.G., Kendall M., Smith D.S., Bassell G.J., Twiss J.L. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol. 2007, 178:965-980.
106. Wool I.G., Chan Y.L., Gluck A. Structure and evolution of mammalian ribosomal proteins. Biochem. Cell Biol. 1995, 73:933-947.
107. Wu K.Y., Hengst U., Cox L.J., Macosko E.Z., Jeromin A., Urquhart E.R., Jaffrey S.R. Local translation of RhoA regulates growth cone collapse. Nature 2005, 436:1020-1024.
108. Yang Y., Fukui K., Koike T., Zheng X. Induction of autophagy in neurite degeneration of mouse superior cervical ganglion neurons. Eur. J. Neurosci. 2007, 26:2979-2988.
109. Yoo S., van Niekerk E.A., Merianda T.T., Twiss J.L. Dynamics of axonal mRNA transport and implications for peripheral nerve regeneration. Exp. Neurol. 2010, 223:19-27.
110. Yoo S., Nguyen M.P., Fukuda M., Bittner G.D., Fishman H.M.. Plasmalemmal sealing of transected mammalian neurites is a gradual process mediated by Ca(2+)-regulated proteins. J. Neurosci. Res. 2003, 74:541-551.
111. Yudin D., Hanz S., Yoo S., Iavnilovitch E., Willis D., Gradus T., Vuppalanchi D., Segal-Ruder Y., Ben-Yaakov K., Hieda M., Yoneda Y., Twiss J.L., Fainzilber M. Localized regulation of axonal RanGTPases controls retrograde injury signaling in peripheral nerve. Neuron 2008, 59:241-252.
112. Yue Z., Wang Q.J., Komatsu M. Neuronal autophagy: going the distance to the axon. Autophagy 2008, 4:94-96.
113. Zanakis M.F., Chakraborty G., Sturman J.A., Ingoglia N.A. Posttranslational protein modification by amino acid addition in intact and regenerating axons of the rat sciatic nerve. J. Neurochem. 1984, 43:1286-1294.
114. Zhang H.L., Eom T., Oleynikov Y., Shenoy S.M., Liebelt D.A., Dictenberg J.B., Singer R.H., Bassell G.J. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 2001, 31:261-275.
115. Zheng J.Q., Kelly T.K., Chang B., Ryazantsev S., Rajasekaran A.K., Martin K.C., Twiss J.L. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. 2001, 21:9291-9303.
116. Zhao Y., Hegde A.N., Martin K.C. The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Curr. Biol. 2003, 13:887-898.
117. Ziv N.E., Spira M.E. Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J. Neurophysiol. 1995, 74:2625-2637.
118. Ziv N.E., Spira M.E. Localized and transient elevations of intracellular Ca2+ induce the dedifferentiation of axonal segments into growth cones. J. Neurosci. 1997, 17:3568-3579.