1932

Abstract

The remit of this review is to give an autobiographical account of our discovery of the role of local protein synthesis in axon guidance. The paper reporting our initial findings was published in 2001. Here, I describe some of the work that led to this publication, the skepticism our findings initially received, and the subsequent exciting years of follow-up work that helped gradually to convince the neuroscience community of the existence and functional importance of local protein synthesis in multiple aspects of axon biology—guidance, branching, synaptogenesis, and maintenance. The journey has been an exhilarating one, taking me into a new field of RNA biology, with many unexpected twists and turns. In retelling it here, I have tried to recall the major influences on my thinking at the time rather than give a comprehensive review, and I apologize for any omissions due to my own ignorance during that era.

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2024-11-25
2025-04-21
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Literature Cited

  1. 1.
    Aakalu G, Smith WB, Jiang C, Nguyen N, Schuman EM. 2001.. Dynamic visualization of dendritic protein synthesis in hippocampal neurons. . Neuron 30::489502
    [Crossref] [Google Scholar]
  2. 2.
    Attardi DG, Sperry RW. 1963.. Preferential selection of central pathways by regenerating optic fibres. . Exp. Neurol. 7::4664
    [Crossref] [Google Scholar]
  3. 3.
    Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, et al. 1998.. Sorting of β-actin mRNA and protein to neurites and growth cones in culture. . J. Neurosci. 18::25165
    [Crossref] [Google Scholar]
  4. 4.
    Bate CM. 1976.. Pioneer neurones in an insect embryo. . Nature 260:(5546):5456
    [Crossref] [Google Scholar]
  5. 5.
    Baumann S, Konig J, Koepke J, Feldbrugge M. 2014.. Endosomal transport of septin mRNA and protein indicates local translation on endosomes and is required for correct septin filamentation. . EMBO Rep. 15::94102
    [Crossref] [Google Scholar]
  6. 6.
    Besse F, Ephrussi A. 2008.. Translational control of localized mRNAs: restricting protein synthesis in space and time. . Nat. Rev. Mol. Cell Biol. 9:(12):97180
    [Crossref] [Google Scholar]
  7. 7.
    Bonhoeffer F, Huf J. 1982.. In vitro experiments on axon guidance demonstrating an anterior-posterior gradient on the tectum. . EMBO J. 1:(4):42731
    [Crossref] [Google Scholar]
  8. 8.
    Brittis PA, Lu Q, Flanagan JG. 2002.. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. . Cell 110::22335
    [Crossref] [Google Scholar]
  9. 9.
    Cagnetta R, Frese CK, Shigeoka T, Krijgsveld J, Holt CE. 2018.. Rapid cue-specific remodeling of the nascent axonal proteome. . Neuron 99:(1):2946
    [Crossref] [Google Scholar]
  10. 10.
    Campbell DS, Holt CE. 2001.. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. . Neuron 32::101326
    [Crossref] [Google Scholar]
  11. 11.
    Campbell DS, Regan AG, Lopez JS, Tannahill D, Harris WA, Holt CE. 2001.. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. . J. Neurosci. 21:(21):853847
    [Crossref] [Google Scholar]
  12. 12.
    Cioni JM, Lin JQ, Holtermann AV, Koppers M, Jakobs MAH, et al. 2019.. Late endosomes act as mRNA translation platforms and sustain mitochondria in axons. . Cell 176:(1–2):5672
    [Crossref] [Google Scholar]
  13. 13.
    Condeelis J, Singer RH. 2005.. How and why does β-actin mRNA target?. Biol. Cell 97:(1):97110
    [Crossref] [Google Scholar]
  14. 14.
    Cosker KE, Fenstermacher SJ, Pazyra-Murphy MF, Elliott HL, Segal RA. 2016.. The RNA-binding protein SFPQ orchestrates an RNA regulon to promote axon viability. . Nat. Neurosci. 19:(5):69096
    [Crossref] [Google Scholar]
  15. 15.
    Crino PB, Eberwine J. 1996.. Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. . Neuron 17:(6):117387
    [Crossref] [Google Scholar]
  16. 16.
    Davis L, Ping D, DeWitt M, Kater SB. 1992.. Protein synthesis within neuronal growth cones. . J. Neurosci. 12::486777
    [Crossref] [Google Scholar]
  17. 17.
    de la Torre JR, Hopker VH, Ming GL, Poo MM, Tessier-Lavigne M, et al. 1997.. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. . Neuron 19::121124
    [Crossref] [Google Scholar]
  18. 18.
    Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Sretavan DW. 1997.. Netrin-1 and DCC mediate axon guidance locally at the optic disc: Loss of function leads to optic nerve hypoplasia. . Neuron 19:(3):57589
    [Crossref] [Google Scholar]
  19. 19.
    Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM. 2006.. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). . PNAS 103:(25):948287
    [Crossref] [Google Scholar]
  20. 20.
    Dodd J, Jessell TM. 1988.. Axon guidance and the patterning of neuronal projections in vertebrates. . Science 242:(4879):69299
    [Crossref] [Google Scholar]
  21. 21.
    Eberwine J. 2001.. Molecular biology of axons: “a turning point…. Neuron 32::95968
    [Crossref] [Google Scholar]
  22. 22.
    Eng H, Lund K, Campenot RB. 1999.. Synthesis of β-tubulin, actin, and other proteins in axons of sympathetic neurons in compartmented cultures. . J. Neurosci. 19::19
    [Crossref] [Google Scholar]
  23. 23.
    Farias J, Holt CE, Sotelo JR, Sotelo-Silveira JR. 2020.. Axon microdissection and transcriptome profiling reveals the in vivo RNA content of fully differentiated myelinated motor axons. . RNA 26:(5):595612
    [Crossref] [Google Scholar]
  24. 24.
    Fusco CM, Desch K, Dörrbaum AR, Wang M, Staab A, et al. 2021.. Neuronal ribosomes exhibit dynamic and context-dependent exchange of ribosomal proteins. . Nat. Commun. 12:(1):6127
    [Crossref] [Google Scholar]
  25. 25.
    Genuth NR, Barna M. 2018.. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. . Mol. Cell 71::36474
    [Crossref] [Google Scholar]
  26. 26.
    Giuditta A, Kaplan BB, van Minnen J, Alvarez J, Koenig E. 2002.. Axonal and presynaptic protein synthesis: new insights into the biology of the neuron. . Trends Neurosci. 25:(8):4004
    [Crossref] [Google Scholar]
  27. 27.
    Glock C, Biever A, Tushev G, Nassim-Assir B, Kao A, et al. 2021.. The translatome of neuronal cell bodies, dendrites, and axons. . PNAS 118:(43):e2113929118
    [Crossref] [Google Scholar]
  28. 28.
    Godement P, Vanselow J, Thanos S, Bonhoeffer F. 1987.. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. . Development 101:(4):697713
    [Crossref] [Google Scholar]
  29. 29.
    Grenningloh G, Rehm EJ, Goodman CS. 1991.. Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. . Cell 67:(1):4557
    [Crossref] [Google Scholar]
  30. 30.
    Gumy LF, Yeo GSH, Tung Y-CL, Zivraj KH, Willis D, et al. 2011.. Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. . RNA 17:(1):8598
    [Crossref] [Google Scholar]
  31. 31.
    Gunderson RW, Barrett JN. 1979.. Neuronal chemotaxis chick dorsal root axons turn toward high concentrations of NGF. . Science 206::107980
    [Crossref] [Google Scholar]
  32. 32.
    Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, et al. 2003.. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. . Neuron 40::1095104
    [Crossref] [Google Scholar]
  33. 33.
    Harris WA. 1986.. Homing behaviour of axons in the embryonic vertebrate brain. . Nature 320:(6059):26669
    [Crossref] [Google Scholar]
  34. 34.
    Harris WA. 1989.. Local positional cues in the neuroepithelium guide retinal axons in embryonic Xenopus brain. . Nature 339:(6221):21821
    [Crossref] [Google Scholar]
  35. 35.
    Harris WA, Holt CE, Bonhoeffer F. 1987.. Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. . Development 101::12333
    [Crossref] [Google Scholar]
  36. 36.
    Harrison RG. 1911.. On the stereotropism of embryonic cells. . Science 34::27981
    [Crossref] [Google Scholar]
  37. 37.
    Heiman M, Schaefer A, Gong S, Peterson JD, Day M, et al. 2008.. A translational profiling approach for the molecular characterization of CNS cell types. . Cell 135::73848
    [Crossref] [Google Scholar]
  38. 38.
    Hillefors M, Gioio AE, Mameza MG, Kaplan BB. 2007.. Axon viability and mitochondrial function are dependent on local protein synthesis in sympathetic neurons. . Cell Mol. Neurobiol. 27:(6):70116
    [Crossref] [Google Scholar]
  39. 39.
    Holt CE. 1982.. The development of the eye and its central connections. PhD Thesis, King's College London:.
    [Google Scholar]
  40. 40.
    Holt CE. 1989.. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. . J. Neurosci. 9:(9):312345
    [Crossref] [Google Scholar]
  41. 41.
    Holt CE, Bullock SL. 2009.. Subcellular mRNA localization in animal cells and why it matters. . Science 326:(5957):121216
    [Crossref] [Google Scholar]
  42. 42.
    Holt CE, Harris WA. 1983.. Order in the initial retinotectal map in Xenopus: a new technique for labelling growing nerve fibres. . Nature 301:(5896):15052
    [Crossref] [Google Scholar]
  43. 43.
    Höpker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C. 1999.. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. . Nature 401:(6748):6973
    [Crossref] [Google Scholar]
  44. 44.
    Huber KM, Kayser MS, Bear MF. 2000.. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. . Science 288:(5469):125457
    [Crossref] [Google Scholar]
  45. 45.
    Job C, Eberwine J. 2001.. Localization and translation of mRNA in dendrites and axons. . Nat. Rev. Neurosci. 2:(12):88998
    [Crossref] [Google Scholar]
  46. 46.
    Jung H, Yoon BC, Holt CE. 2012.. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. . Nat. Rev. Neurosci. 13:(5):30824
    [Crossref] [Google Scholar]
  47. 47.
    Kang H, Schuman EM. 1996.. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. . Science 273:(5280):14026
    [Crossref] [Google Scholar]
  48. 48.
    Kapfhammer JP, Raper JA. 1987.. Collapse of growth cone structure on contact with specific neurites in culture. . J. Neurosci. 7:(1):20112
    [Crossref] [Google Scholar]
  49. 49.
    Kaplan BB, Gioio AE, Capano CP, Crispino M, Giuditta A. 1992.. β-Actin and β-Tubulin are components of a heterogeneous mRNA population present in the squid giant axon. . Mol. Cell. Neurosci. 3:(2):13344
    [Crossref] [Google Scholar]
  50. 50.
    Kislauskis E, Zhu X, Singer R. 1997.. β-Actin messenger RNA localization and protein synthesis augment cell motility. . J. Cell Biol. 136::126370
    [Crossref] [Google Scholar]
  51. 51.
    Koenig E. 1967.. Synthetic mechanisms in the axon—IV. In vitro incorporation of [3H]precursors into axonal protein and RNA. . J. Neurochem. 14::43746
    [Crossref] [Google Scholar]
  52. 52.
    Koenig E, Giuditta A. 1999.. Protein-synthesizing machinery in the axon compartment. . Neuroscience 89::515
    [Crossref] [Google Scholar]
  53. 53.
    Lance-Jones C, Landmesser L. 1980.. Motoneurone projection patterns in the chick hind limb following early partial reversals of the spinal cord. . J. Physiol. 302::581602
    [Crossref] [Google Scholar]
  54. 54.
    Lance-Jones C, Landmesser L. 1981.. Pathway selection by chick lumbosacral motoneurons during normal development. . Proc. R. Soc. Lond. B 214:(1194):118
    [Crossref] [Google Scholar]
  55. 55.
    Lee SK, Hollenbeck PJ. 2003.. Organization and translation of mRNA in sympathetic axons. . J. Cell Sci. 116::446778
    [Crossref] [Google Scholar]
  56. 56.
    Leung KM, Holt CE. 2008.. Live visualization of protein synthesis in axonal growth cones by microinjection of photoconvertible Kaede into Xenopus embryos. . Nat. Protoc. 3::131827
    [Crossref] [Google Scholar]
  57. 57.
    Leung KM, Lu B, Wong HH, Lin JQ, Turner-Bridger B, Holt CE. 2018.. Cue-polarized transport of β-actin mRNA depends on 3′UTR and microtubules in live growth cones. . Front. Cell Neurosci. 12::300
    [Crossref] [Google Scholar]
  58. 58.
    Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE. 2006.. Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1. . Nat. Neurosci. 9:(10):124756
    [Crossref] [Google Scholar]
  59. 59.
    Lin AC, Holt CE. 2007.. Local translation and directional steering in axons. . EMBO J. 26:(16):372936
    [Crossref] [Google Scholar]
  60. 60.
    Lin AC, Holt CE. 2008.. Function and regulation of local axonal translation. . Curr. Opin. Neurobiol. 18::6068
    [Crossref] [Google Scholar]
  61. 61.
    Litman P, Barg J, Rindzoonski L, Ginzburg I. 1993.. Subcellular localization of tau mRNA in differentiating neuronal cell culture: implications for neuronal polarity. . Neuron 10::62738
    [Crossref] [Google Scholar]
  62. 62.
    Lohof AM, Quillan M, Dan Y, Poo MM. 1992.. Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. . J. Neurosci. 12::125361
    [Crossref] [Google Scholar]
  63. 63.
    Martin KC, Casadio A, Zhu H, E Y, Rose JC, et al. 1997.. Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. . Cell 91:(7):92738
    [Crossref] [Google Scholar]
  64. 64.
    Ming GL, Wong ST, Henley J, Yuan XB, Song HJ, et al. 2002.. Adaptation in the chemotactic guidance of nerve growth cones. . Nature 417::41118
    [Crossref] [Google Scholar]
  65. 65.
    Moccia R, Chen D, Lyles V, Kapuya E, E Y, et al. 2003.. An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. . J. Neurosci. 23:(28):940917
    [Crossref] [Google Scholar]
  66. 66.
    Olink-Coux M, Hollenbeck PJ. 1996.. Localization and active transport of mRNA in axons of sympathetic neurons in culture. . J. Neurosci. 16::134658
    [Crossref] [Google Scholar]
  67. 67.
    Palacios IM, St. Johnston D. 2001.. Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. . Annu. Rev. Cell Dev. Biol. 17::569614
    [Crossref] [Google Scholar]
  68. 68.
    Piper M, Anderson R, Dwivedy A, Weinl C, van Horck F, et al. 2006.. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. . Neuron 49::21528
    [Crossref] [Google Scholar]
  69. 69.
    Piper M, Dwivedy A, Leung L, Bradley RS, Holt CE. 2008.. NF-protocadherin and TAF1 regulate retinal axon initiation and elongation in vivo. . J. Neurosci. 28:(1):1005
    [Crossref] [Google Scholar]
  70. 70.
    Piper M, Salih S, Weinl C, Holt CE, Harris WA. 2005.. Endocytosis-dependent desensitization and protein synthesis–dependent resensitization in retinal growth cone adaptation. . Nat. Neurosci. 8::17986
    [Crossref] [Google Scholar]
  71. 71.
    Ramón y Cajal S. 1890.. A quelle époque aparaissent les expansions des cellule nerveuses de la moelle épinière du poulet. . Anatom. Anzeiger 5::60913
    [Google Scholar]
  72. 72.
    Ramón y Cajal S. 1937.. Recollections of My Life, transl. EH Craigie, J Cano . Cambridge, MA:: MIT Press
    [Google Scholar]
  73. 73.
    Raper JA, Bastiani M, Goodman CS. 1983.. Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by the growth cones of sibling neurons. . J. Neurosci. 3:(1):2030
    [Crossref] [Google Scholar]
  74. 74.
    Scholes JH. 1979.. Nerve fibre topography in the retinal projection to the tectum. . Nature 278:(5705):62024
    [Crossref] [Google Scholar]
  75. 75.
    Schwartz JH, DeCamilli P. 2000.. Synthesis and trafficking of neuronal protein. . In Principles of Neural Science, ed. ER Kandel, JH Schwartz, TM Jessell , pp. 88104. New York:: McGraw-Hill
    [Google Scholar]
  76. 76.
    Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M. 1994.. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. . Cell 78:(3):40924
    [Crossref] [Google Scholar]
  77. 77.
    Shaw G, Bray D. 1977.. Movement and extension of isolated growth cones. . Exp. Cell Res. 104::5562
    [Crossref] [Google Scholar]
  78. 78.
    Shestakova EA, Singer RH, Condeelis J. 2001.. The physiological significance of β-actin mRNA localization in determining cell polarity and directional motility. . PNAS 98::704550
    [Crossref] [Google Scholar]
  79. 79.
    Shigeoka T, Jung H, Jung J, Turner-Bridger B, Ohk J, et al. 2016.. Dynamic axonal translation in developing and mature visual circuits. . Cell 166:(1):18192
    [Crossref] [Google Scholar]
  80. 80.
    Shigeoka T, Jung J, Holt CE, Jung H. 2018.. Axon-TRAP-RiboTag: affinity purification of translated mRNAs from neuronal axons in mouse in vivo. . Methods Mol. Biol. 1649::8594
    [Crossref] [Google Scholar]
  81. 81.
    Shigeoka T, Koppers M, Wong HH, Lin JQ, Cagnetta R, et al. 2019.. On-site ribosome remodeling by locally synthesized ribosomal proteins in axons. . Cell Rep. 29:(11):360519.e10
    [Crossref] [Google Scholar]
  82. 82.
    Song HJ, Ming GL, Poo MM. 1997.. cAMP-induced switching in turning direction of nerve growth cones. . Nature 388:(6639):27579
    [Crossref] [Google Scholar]
  83. 83.
    Sotelo-Silveira JR, Calliari A, Kun A, Benech JC, Sanguinetti C, et al. 2000.. Neurofilament mRNAs are present and translated in the normal and severed sciatic nerve. . J. Neurosci. Res. 62::6574
    [Crossref] [Google Scholar]
  84. 84.
    Speidel CC. 1948.. Growth of nerve fibers as revealed by fast motion cine photomicrography. . Anat. Rec. 101:(4):697
    [Google Scholar]
  85. 85.
    Steward O, Levy WB. 1982.. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. . J. Neurosci. 2::28491
    [Crossref] [Google Scholar]
  86. 86.
    Taghert PH, Bastiani MJ, Ho RK, Goodman CS. 1982.. Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. . Dev. Biol. 94:(2):39199
    [Crossref] [Google Scholar]
  87. 87.
    Tennyson VM. 1970.. The fine structure of the axon and growth cone of the dorsal root neuroblast of the rabbit embryo. . J. Cell Biol. 44::6279
    [Crossref] [Google Scholar]
  88. 88.
    Tessier-Lavigne M, Goodman CS. 1996.. The molecular biology of axon guidance. . Science 274::112333
    [Crossref] [Google Scholar]
  89. 89.
    Tessier-Lavigne M, Placzek M, Lumsden AG, Dodd J, Jessell TM. 1988.. Chemotropic guidance of developing axons in the mammalian central nervous system. . Nature 336:(6201):77578
    [Crossref] [Google Scholar]
  90. 90.
    Torre ER, Steward O. 1992.. Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies. . J. Neurosci. 12:(3):76272
    [Crossref] [Google Scholar]
  91. 91.
    Tosney KW, Landmesser LT. 1985.. Specificity of early motoneuron growth cone outgrowth in the chick embryo. . J. Neurosci. 5:(9):233644
    [Crossref] [Google Scholar]
  92. 92.
    Trembleau A, Morales M, Bloom FE. 1996.. Differential compartmentalization of vasopressin messenger RNA and neuropeptide within the rat hypothalamo-neurohypophysial axonal tracts: light and electron microscopic evidence. . Neuroscience 70::11325
    [Crossref] [Google Scholar]
  93. 93.
    Turner-Bridger B, Jakobs M, Muresan L, Wong HH, Franze K, et al. 2018.. Single-molecule analysis of endogenous β-actin mRNA trafficking reveals a mechanism for compartmentalized mRNA localization in axons. . PNAS 115:(41):E9697706
    [Crossref] [Google Scholar]
  94. 94.
    Van Minnen J, Bergman JJ, Van Kesteren ER, Smit AB, Geraerts WP, et al. 1997.. De novo protein synthesis in isolated axons of identified neurons. . Neuroscience 80:(1):17
    [Crossref] [Google Scholar]
  95. 95.
    Weiss P. 1937.. Further experimental investigations on the phenomenon of homologous response in transplanted amphibian limbs. II. Nerve regeneration and the innervation of transplanted limbs. . J. Comp. Neurol. 66::481535
    [Crossref] [Google Scholar]
  96. 96.
    Willis D, Li KW, Zheng JQ, Chang JH, Smit A, et al. 2005.. Differential transport and local translation of cytoskeletal, injury-response, and neurodegeneration protein mRNAs in axons. . J. Neurosci. 25::77891
    [Crossref] [Google Scholar]
  97. 97.
    Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT, et al. 2007.. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. . J. Cell Biol. 178::96580
    [Crossref] [Google Scholar]
  98. 98.
    Wong HH-W, Lin JQ, Ströhl F, Roque CG, Cioni JM, et al. 2017.. RNA docking and local translation regulate site-specific axon remodeling in vivo. . Neuron 95:(4):85268.e8
    [Crossref] [Google Scholar]
  99. 99.
    Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, et al. 2005.. Local translation of RhoA regulates growth cone collapse. . Nature 436::102024
    [Crossref] [Google Scholar]
  100. 100.
    Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ. 2006.. An essential role for β-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. . Nat. Neurosci. 9::126573
    [Crossref] [Google Scholar]
  101. 101.
    Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE. 2012.. Local translation of extranuclear lamin B promotes axon maintenance. . Cell 148:(4):75264
    [Crossref] [Google Scholar]
  102. 102.
    Zelenà J. 1970.. Ribosome-like particles in myelinated axons of the rat. . Brain Res. 24::35963
    [Crossref] [Google Scholar]
  103. 103.
    Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, et al. 2001.. Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility. . Neuron 31::26175
    [Crossref] [Google Scholar]
  104. 104.
    Zhang HL, Singer RH, Bassell GJ. 1999.. Neurotrophin regulation of β-actin mRNA and protein localization within growth cones. . J. Cell Biol. 147::5970
    [Crossref] [Google Scholar]
  105. 105.
    Zheng JQ, Kelly TK, Chang B, Ryanzantsev S, Rajasekaran AK, et al. 2001.. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. . J. Neurosci. 21::9291303
    [Crossref] [Google Scholar]
  106. 106.
    Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, et al. 2010.. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. . J. Neurosci. 30:(46):1546478
    [Crossref] [Google Scholar]
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