1932

Abstract

Axons receive extracellular signals that help to guide growth and synapse formation during development and to maintain neuronal function and survival during maturity. These signals relay information via cell surface receptors that can initiate local intracellular signaling at the site of binding, including local messenger RNA (mRNA) translation. Direct coupling of translational machinery to receptors provides an attractive way to activate this local mRNA translation and change the local proteome with high spatiotemporal resolution. Here, we first discuss the increasing evidence that different external stimuli trigger translation of specific subsets of mRNAs in axons via receptors and thus play a prominent role in various processes in both developing and mature neurons. We then discuss the receptor-mediated molecular mechanisms that regulate local mRNA translation with a focus on direct receptor-ribosome coupling. We advance the idea that receptor-ribosome coupling provides several advantages over other translational regulation mechanisms and is a common mechanism in cell communication.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-083021-110015
2022-07-08
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/neuro/45/1/annurev-neuro-083021-110015.html?itemId=/content/journals/10.1146/annurev-neuro-083021-110015&mimeType=html&fmt=ahah

Literature Cited

  1. Alvarez J, Giuditta A, Koenig E 2000. Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol. 62:1–62
    [Google Scholar]
  2. Alvarez-Castelao B, tom Dieck S, Fusco CM, Donlin-Asp P, Perez JD, Schuman EM 2020. The switch-like expression of heme-regulated kinase 1 mediates neuronal proteostasis following proteasome inhibition. eLife 9:e52714
    [Google Scholar]
  3. Andreassi C, Zimmermann C, Mitter R, Fusco S, De Vita S et al. 2010. An NGF-responsive element targets myo-inositol monophosphatase-1 mRNA to sympathetic neuron axons. Nat. Neurosci. 13:291–301
    [Google Scholar]
  4. Aschrafi A, Schwechter AD, Mameza MG, Natera-Naranjo O, Gioio AE, Kaplan BB. 2008. MicroRNA-338 regulates local cytochrome c oxidase IV mRNA levels and oxidative phosphorylation in the axons of sympathetic neurons. J. Neurosci. 28:12581–90
    [Google Scholar]
  5. Batista AF, Hengst U. 2016. Intra-axonal protein synthesis in development and beyond. Int. J. Dev. Neurosci. 55:140–49
    [Google Scholar]
  6. Batista AFR, Martinez JC, Hengst U. 2017. Intra-axonal synthesis of SNAP25 is required for the formation of presynaptic terminals. Cell Rep. 20:3085–98
    [Google Scholar]
  7. Bellon A, Iyer A, Bridi S, Lee FCY, Ovando-Vazquez C et al. 2017. miR-182 regulates Slit2-mediated axon guidance by modulating the local translation of a specific mRNA. Cell Rep. 18:1171–86
    [Google Scholar]
  8. Biever A, Glock C, Tushev G, Ciirdaeva E, Dalmay T et al. 2020. Monosomes actively translate synaptic mRNAs in neuronal processes. Science 367:aay4991
    [Google Scholar]
  9. Brittis PA, Lu Q, Flanagan JG 2002. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223–35
    [Google Scholar]
  10. Brunet I, Weinl C, Piper M, Trembleau A, Volovitch M et al. 2005. The transcription factor Engrailed-2 guides retinal axons. Nature 438:706494–98
    [Google Scholar]
  11. Buxbaum AR, Haimovich G, Singer RH. 2015a. In the right place at the right time: visualizing and understanding mRNA localization. Nat. Rev. Mol. Cell Biol. 16:95–109
    [Google Scholar]
  12. Buxbaum AR, Wu B, Singer RH. 2014. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343:419–22
    [Google Scholar]
  13. Buxbaum AR, Yoon YJ, Singer RH, Park HY. 2015b. Single-molecule insights into mRNA dynamics in neurons. Trends Cell Biol. 25:468–75
    [Google Scholar]
  14. Cagnetta R, Frese CK, Shigeoka T, Krijgsveld J, Holt CE 2018. Rapid cue-specific remodeling of the nascent axonal proteome. Neuron 99:29–46.e4
    [Google Scholar]
  15. Cagnetta R, Wong HH, Frese CK, Mallucci GR, Krijgsveld J, Holt CE 2019. Noncanonical modulation of the eIF2 pathway controls an increase in local translation during neural wiring. Mol. Cell 73:474–89.e5
    [Google Scholar]
  16. Cajigas IJ, Tushev G, Will TJ, tom Dieck S, Fuerst N, Schuman EM 2012. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74:453–66
    [Google Scholar]
  17. Campbell DS, Holt CE. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013–26
    [Google Scholar]
  18. Campbell DS, Holt CE. 2003. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37:939–52
    [Google Scholar]
  19. 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. 21:8538–47
    [Google Scholar]
  20. Chedotal A. 2019. Roles of axon guidance molecules in neuronal wiring in the developing spinal cord. Nat. Rev. Neurosci. 20:380–96
    [Google Scholar]
  21. Cioni JM, Koppers M, Holt CE. 2018. Molecular control of local translation in axon development and maintenance. Curr. Opin. Neurobiol. 51:86–94
    [Google Scholar]
  22. 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 176:56–72.e15
    [Google Scholar]
  23. Colak D, Ji SJ, Porse BT, Jaffrey SR. 2013. Regulation of axon guidance by compartmentalized nonsense-mediated mRNA decay. Cell 153:1252–65
    [Google Scholar]
  24. Corradi E, Baudet ML 2020. In the right place at the right time: miRNAs as key regulators in developing axons. Int. J. Mol. Sci. 21:8726
    [Google Scholar]
  25. Corradi E, Dalla Costa I, Gavoci A, Iyer A, Roccuzzo M et al. 2020. Axonal precursor miRNAs hitchhike on endosomes and locally regulate the development of neural circuits. EMBO J. 39:e102513
    [Google Scholar]
  26. 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. 19:690–96
    [Google Scholar]
  27. Cosker KE, Pazyra-Murphy MF, Fenstermacher SJ, Segal RA 2013. Target-derived neurotrophins coordinate transcription and transport of Bclw to prevent axonal degeneration. J. Neurosci. 33:5195–207
    [Google Scholar]
  28. Costa CJ, Willis DE. 2018. To the end of the line: axonal mRNA transport and local translation in health and neurodegenerative disease. Dev. Neurobiol. 78:209–20
    [Google Scholar]
  29. Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR. 2008. Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat. Cell Biol. 10:149–59
    [Google Scholar]
  30. Crerar H, Scott-Solomon E, Bodkin-Clarke C, Andreassi C, Hazbon M et al. 2019. Regulation of NGF signaling by an axonal untranslated mRNA. Neuron 102:553–63.e8
    [Google Scholar]
  31. Das S, Vera M, Gandin V, Singer RH, Tutucci E. 2021. Intracellular mRNA transport and localized translation. Nat. Rev. Mol. Cell Biol. 22:483–504
    [Google Scholar]
  32. de Hoog CL, Foster LJ, Mann M. 2004. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 117:649–62
    [Google Scholar]
  33. Deglincerti A, Liu Y, Colak D, Hengst U, Xu G, Jaffrey SR. 2015. Coupled local translation and degradation regulate growth cone collapse. Nat. Commun. 6:6888
    [Google Scholar]
  34. Donlin-Asp PG, Polisseni C, Klimek R, Heckel A, Schuman EM. 2021. Differential regulation of local mRNA dynamics and translation following long-term potentiation and depression. PNAS 118:e2017578118
    [Google Scholar]
  35. Dorskind JM, Kolodkin AL. 2020. Revisiting and refining roles of neural guidance cues in circuit assembly. Curr. Opin. Neurobiol. 66:10–21
    [Google Scholar]
  36. Dudanova I, Klein R. 2013. Integration of guidance cues: parallel signaling and crosstalk. Trends Neurosci. 36:295–304
    [Google Scholar]
  37. 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. 19:1–9
    [Google Scholar]
  38. Fazal FM, Han S, Parker KR, Kaewsapsak P, Xu J et al. 2019. Atlas of subcellular RNA localization revealed by APEX-Seq. Cell 178:473–90.e26
    [Google Scholar]
  39. Formicola N, Heim M, Dufourt J, Lancelot AS, Nakamura A et al. 2021. Tyramine induces dynamic RNP granule remodeling and translation activation in the Drosophila brain. eLife 10:e65742
    [Google Scholar]
  40. Formicola N, Vijayakumar J, Besse F. 2019. Neuronal ribonucleoprotein granules: dynamic sensors of localized signals. Traffic 20:639–49
    [Google Scholar]
  41. 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 126127
    [Google Scholar]
  42. Gabanella F, Onori A, Ralli M, Greco A, Passananti C, Di Certo MG. 2020. SMN protein promotes membrane compartmentalization of ribosomal protein S6 transcript in human fibroblasts. Sci. Rep. 10:19000
    [Google Scholar]
  43. Genuth NR, Barna M. 2018. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. Mol. Cell 71:364–74
    [Google Scholar]
  44. Gershoni-Emek N, Altman T, Ionescu A, Costa CJ, Gradus-Pery T et al. 2018. Localization of RNAi machinery to axonal branch points and growth cones is facilitated by mitochondria and is disrupted in ALS. Front. Mol. Neurosci. 11:311
    [Google Scholar]
  45. Glasgow SD, Wong EW, Thompson-Steckel G, Marcal N, Seguela P et al. 2020. Pre- and post-synaptic roles for DCC in memory consolidation in the adult mouse hippocampus. Mol. Brain. 13:56
    [Google Scholar]
  46. Gomez TM, Zheng JQ. 2006. The molecular basis for calcium-dependent axon pathfinding. Nat. Rev. Neurosci. 7:115–25
    [Google Scholar]
  47. Gonzalez C, Canovas J, Fresno J, Couve E, Court FA, Couve A 2016. Axons provide the secretory machinery for trafficking of voltage-gated sodium channels in peripheral nerve. PNAS 113:1823–28
    [Google Scholar]
  48. Gouveia Roque C, Holt CE 2018. Growth cone Tctp is dynamically regulated by guidance cues. 11399
  49. Gracias NG, Shirkey-Son NJ, Hengst U. 2014. Local translation of TC10 is required for membrane expansion during axon outgrowth. Nat. Commun. 5:3506
    [Google Scholar]
  50. Hafner A-S, Donlin-Asp PG, Leitch B, Herzog E, Schuman EM. 2019. Local protein synthesis is a ubiquitous feature of neuronal pre- and postsynaptic compartments. Science 364:eaau3644
    [Google Scholar]
  51. 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 101:123–33
    [Google Scholar]
  52. Hengst U, Deglincerti A, Kim HJ, Jeon NL, Jaffrey SR 2009. Axonal elongation triggered by stimulus-induced local translation of a polarity complex protein. Nat. Cell Biol. 11:1024–30
    [Google Scholar]
  53. Heyer EE, Moore MJ. 2016. Redefining the translational status of 80S monosomes. Cell 164:757–69
    [Google Scholar]
  54. Hopker 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 401:69–73
    [Google Scholar]
  55. Horn KE, Glasgow SD, Gobert D, Bull SJ, Luk T et al. 2013. DCC expression by neurons regulates synaptic plasticity in the adult brain. Cell Rep. 3:173–85
    [Google Scholar]
  56. Hsiao K, Bozdagi O, Benson DL. 2014. Axonal cap-dependent translation regulates presynaptic p35. Dev. Neurobiol. 74:351–64
    [Google Scholar]
  57. Hüttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M et al. 2005. Spatial regulation of β-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438:512–15
    [Google Scholar]
  58. Jung H, Gkogkas CG, Sonenberg N, Holt CE. 2014. Remote control of gene function by local translation. Cell 157:26–40
    [Google Scholar]
  59. Jung H, Yoon BC, Holt CE. 2012. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat. Rev. Neurosci. 13:308–24
    [Google Scholar]
  60. Kalil K, Dent EW 2014. Branch management: mechanisms of axon branching in the developing vertebrate CNS. Nat. Rev. Neurosci. 15:7–18
    [Google Scholar]
  61. Klein U, Ramirez MT, Kobilka BK, von Zastrow M. 1997. A novel interaction between adrenergic receptors and the α-subunit of eukaryotic initiation factor 2B. J. Biol. Chem. 272:19099–102
    [Google Scholar]
  62. Koenig E, Martin R. 1996. Cortical plaque-like structures identify ribosome-containing domains in the Mauthner cell axon. J. Neurosci. 16:1400–11
    [Google Scholar]
  63. Kolodkin AL, Tessier-Lavigne M. 2011. Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3:a001727
    [Google Scholar]
  64. Koppers M, Cagnetta R, Shigeoka T, Wunderlich LC, Vallejo-Ramirez P et al. 2019. Receptor-specific interactome as a hub for rapid cue-induced selective translation in axons. eLife 8:e48718
    [Google Scholar]
  65. Kun A, Otero L, Sotelo-Silveira JR, Sotelo JR. 2007. Ribosomal distributions in axons of mammalian myelinated fibers. J. Neurosci. Res. 85:2087–98
    [Google Scholar]
  66. Kundel M, Jones KJ, Shin CY, Wells DG. 2009. Cytoplasmic polyadenylation element-binding protein regulates neurotrophin-3-dependent β-catenin mRNA translation in developing hippocampal neurons. J. Neurosci. 29:4313630–39
    [Google Scholar]
  67. Lam SS, Martell JD, Kamer KJ, Deerinck TJ, Ellisman MH et al. 2015. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12:51–54
    [Google Scholar]
  68. Larrieu-Lahargue F, Thomas KR, Li DY 2012. Netrin ligands and receptors: lessons from neurons to the endothelium. Trends Cardiovasc. Med. 22:44–47
    [Google Scholar]
  69. Lee AS, Kranzusch PJ, Doudna JA, Cate JH. 2016. eIF3d is an mRNA cap-binding protein that is required for specialized translation initiation. Nature 536:96–99
    [Google Scholar]
  70. Lepelletier L, Langlois SD, Kent CB, Welshhans K, Morin S et al. 2017. Sonic hedgehog guides axons via zipcode binding protein 1-mediated local translation. J. Neurosci. 37:1685–95
    [Google Scholar]
  71. 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. 9:1247–56
    [Google Scholar]
  72. Li Y, Massey K, Witkiewicz H, Schnitzer JE. 2011. Systems analysis of endothelial cell plasma membrane proteome of rat lung microvasculature. Proteome Sci. 9:15
    [Google Scholar]
  73. Liao YC, Fernandopulle MS, Wang G, Choi H, Hao L et al. 2019. RNA granules hitchhike on lysosomes for long-distance transport, using annexin A11 as a molecular tether. Cell 179:147–64.e20
    [Google Scholar]
  74. Manitt C, Nikolakopoulou AM, Almario DR, Nguyen SA, Cohen-Cory S. 2009. Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain. J. Neurosci. 29:11065–77
    [Google Scholar]
  75. Mann F, Miranda E, Weinl C, Harmer E, Holt CE. 2003. B-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J. Neurobiol. 57:323–36
    [Google Scholar]
  76. Manns RP, Cook GM, Holt CE, Keynes RJ. 2012. Differing semaphorin 3A concentrations trigger distinct signaling mechanisms in growth cone collapse. J. Neurosci. 32:8554–59
    [Google Scholar]
  77. Merkurjev D, Hong WT, Iida K, Oomoto I, Goldie BJ et al. 2018. Synaptic N6-methyladenosine (m6A) epitranscriptome reveals functional partitioning of localized transcripts. Nat. Neurosci. 21:1004–14
    [Google Scholar]
  78. Ming GL, Wong ST, Henley J, Yuan XB, Song HJ et al. 2002. Adaptation in the chemotactic guidance of nerve growth cones. Nature 417:411–18
    [Google Scholar]
  79. Minis A, Dahary D, Manor O, Leshkowitz D, Pilpel Y, Yaron A. 2014. Subcellular transcriptomics—dissection of the mRNA composition in the axonal compartment of sensory neurons. Dev. Neurobiol. 74:365–81
    [Google Scholar]
  80. Morales D, Kania A. 2017. Cooperation and crosstalk in axon guidance cue integration: additivity, synergy, and fine-tuning in combinatorial signaling. Dev. Neurobiol. 77:891–904
    [Google Scholar]
  81. Morisaki T, Lyon K, DeLuca KF, DeLuca JG, English BP et al. 2016. Real-time quantification of single RNA translation dynamics in living cells. Science 352:1425–29
    [Google Scholar]
  82. Nagano S, Jinno J, Abdelhamid RF, Jin Y, Shibata M et al. 2020. TDP-43 transports ribosomal protein mRNA to regulate axonal local translation in neuronal axons. Acta Neuropathol. 140:695–713
    [Google Scholar]
  83. Natera-Naranjo O, Kar AN, Aschrafi A, Gervasi NM, Macgibeny MA et al. 2012. Local translation of ATP synthase subunit 9 mRNA alters ATP levels and the production of ROS in the axon. Mol. Cell Neurosci. 49:263–70
    [Google Scholar]
  84. Nedelec S, Peljto M, Shi P, Amoroso MW, Kam LC, Wichterle H 2012. Concentration-dependent requirement for local protein synthesis in motor neuron subtype-specific response to axon guidance cues. J. Neurosci. 32:1496–506
    [Google Scholar]
  85. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32:701–12
    [Google Scholar]
  86. Nie D, Di Nardo A, Han JM, Baharanyi H, Kramvis I et al. 2010. Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat. Neurosci. 13:163–72
    [Google Scholar]
  87. Ohashi R, Shiina N. 2020. Cataloguing and selection of mRNAs localized to dendrites in neurons and regulated by RNA-binding proteins in RNA granules. Biomolecules 10:167
    [Google Scholar]
  88. Ostroff LE, Santini E, Sears R, Deane Z, Kanadia RN et al. 2019. Axon TRAP reveals learning-associated alterations in cortical axonal mRNAs in the lateral amgydala. eLife 8:e51607
    [Google Scholar]
  89. Palmesino E, Apuzzo T, Thelen S, Mueller B, Langen H, Thelen M. 2016. Association of eukaryotic translation initiation factor eIF2B with fully solubilized CXCR4. J. Leukoc. Biol. 99:971–78
    [Google Scholar]
  90. Parvin S, Takeda R, Sugiura Y, Neyazaki M, Nogi T, Sasaki Y 2019. Fragile X mental retardation protein regulates accumulation of the active zone protein Munc18-1 in presynapses via local translation in axons during synaptogenesis. Neurosci. Res. 146:36–47
    [Google Scholar]
  91. Pasterkamp RJ, Burk K. 2021. Axon guidance receptors: endocytosis, trafficking and downstream signaling from endosomes. Prog. Neurobiol. 198:101916
    [Google Scholar]
  92. Pichon X, Bastide A, Safieddine A, Chouaib R, Samacoits A et al. 2016. Visualization of single endogenous polysomes reveals the dynamics of translation in live human cells. J. Cell Biol. 214:769–81
    [Google Scholar]
  93. 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 49:215–28
    [Google Scholar]
  94. 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. 8:179–86
    [Google Scholar]
  95. Poliak S, Morales D, Croteau LP, Krawchuk D, Palmesino E et al. 2015. Synergistic integration of Netrin and ephrin axon guidance signals by spinal motor neurons. eLife 4:e10841
    [Google Scholar]
  96. Poulopoulos A, Murphy AJ, Ozkan A, Davis P, Hatch J et al. 2019. Subcellular transcriptomes and proteomes of developing axon projections in the cerebral cortex. Nature 565:356–60
    [Google Scholar]
  97. Preitner N, Quan J, Nowakowski DW, Hancock ML, Shi J et al. 2014. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 158:368–82
    [Google Scholar]
  98. Ramachandran KV, Fu JM, Schaffer TB, Na CH, Delannoy M, Margolis SS 2018. Activity-dependent degradation of the nascentome by the neuronal membrane proteasome. Mol. Cell 71:169–77.e6
    [Google Scholar]
  99. Ramachandran KV, Margolis SS. 2017. A mammalian nervous-system-specific plasma membrane proteasome complex that modulates neuronal function. Nat. Struct. Mol. Biol. 24:419–30
    [Google Scholar]
  100. Rodriguez J, Esteve P, Weinl C, Ruiz JM, Fermin Y et al. 2005. SFRP1 regulates the growth of retinal ganglion cell axons through the Fz2 receptor. Nat. Neurosci. 8:101301–9
    [Google Scholar]
  101. Roy S, Bag AK, Singh RK, Talmadge JE, Batra SK, Datta K. 2017. Multifaceted role of neuropilins in the immune system: potential targets for immunotherapy. Front. Immunol. 8:1228
    [Google Scholar]
  102. Russell SA, Bashaw GJ. 2018. Axon guidance pathways and the control of gene expression. Dev. Dyn. 247:571–80
    [Google Scholar]
  103. Sasaki Y, Welshhans K, Wen Z, Yao J, Xu M et al. 2010. Phosphorylation of zipcode binding protein 1 is required for brain-derived neurotrophic factor signaling of local β-actin synthesis and growth cone turning. J. Neurosci. 30:9349–58
    [Google Scholar]
  104. Saxton RA, Sabatini DM. 2017. mTOR signaling in growth, metabolism, and disease. Cell 169:361–71
    [Google Scholar]
  105. Scarnati MS, Kataria R, Biswas M, Paradiso KG 2018. Active presynaptic ribosomes in the mammalian brain, and altered transmitter release after protein synthesis inhibition. eLife 7:e36697
    [Google Scholar]
  106. Shen K, Cowan CW. 2010. Guidance molecules in synapse formation and plasticity. Cold Spring Harb. Perspect. Biol. 2:a001842
    [Google Scholar]
  107. Shewan D, Dwivedy A, Anderson R, Holt CE 2002. Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat. Neurosci. 5:955–62
    [Google Scholar]
  108. Shigeoka T, Jung H, Jung J, Turner-Bridger B, Ohk J et al. 2016. Dynamic axonal translation in developing and mature visual circuits. Cell 166:181–92
    [Google Scholar]
  109. 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. 29:3605–19.e10
    [Google Scholar]
  110. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731–45
    [Google Scholar]
  111. Spillane M, Ketschek A, Donnelly CJ, Pacheco A, Twiss JL, Gallo G. 2012. Nerve growth factor-induced formation of axonal filopodia and collateral branches involves the intra-axonal synthesis of regulators of the actin-nucleating Arp2/3 complex. J. Neurosci. 32:17671–89
    [Google Scholar]
  112. Spillane M, Ketschek A, Merianda TT, Twiss JL, Gallo G. 2013. Mitochondria coordinate sites of axon branching through localized intra-axonal protein synthesis. Cell Rep. 5:1564–75
    [Google Scholar]
  113. Stoeckli ET. 2018. Understanding axon guidance: Are we nearly there yet?. Development 145:dev151415
    [Google Scholar]
  114. Taylor AM, Berchtold NC, Perreau VM, Tu CH, Jeon NL, Cotman CW 2009. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29:4697–707
    [Google Scholar]
  115. Taylor AM, Wu J, Tai HC, Schuman EM 2013. Axonal translation of β-catenin regulates synaptic vesicle dynamics. J. Neurosci. 33:5584–89
    [Google Scholar]
  116. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG. 2010. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141:632–44
    [Google Scholar]
  117. Terenzio M, Koley S, Samra N, Rishal I, Zhao Q et al. 2018. Locally translated mTOR controls axonal local translation in nerve injury. Science 359:1416–21
    [Google Scholar]
  118. Terenzio M, Schiavo G, Fainzilber M. 2017. Compartmentalized signaling in neurons: from cell biology to neuroscience. Neuron 96:667–79
    [Google Scholar]
  119. Tojima T, Hines JH, Henley JR, Kamiguchi H. 2011. Second messengers and membrane trafficking direct and organize growth cone steering. Nat. Rev. Neurosci. 12:191–203
    [Google Scholar]
  120. Turner-Bridger B, Caterino C, Cioni JM 2020. Molecular mechanisms behind mRNA localization in axons. Open Biol. 10:200177
    [Google Scholar]
  121. Vallecillo-Viejo IC, Liscovitch-Brauer N, Diaz Quiroz JF, Montiel-Gonzalez MF, Nemes SE et al. 2020. Spatially regulated editing of genetic information within a neuron. Nucleic Acids Res. 48:3999–4012
    [Google Scholar]
  122. Villarin JM, McCurdy EP, Martinez JC, Hengst U. 2016. Local synthesis of dynein cofactors matches retrograde transport to acutely changing demands. Nat. Commun. 7:13865
    [Google Scholar]
  123. Walker BA, Ji SJ, Jaffery SR 2012. Intra-axonal translation of RhoA promotes axon growth inhibition by CSPG. J. Neurosci. 32:4114442–47
    [Google Scholar]
  124. Wang B, Bao L. 2017. Axonal microRNAs: localization, function and regulatory mechanism during axon development. J. Mol. Cell Biol. 9:82–90
    [Google Scholar]
  125. Willems J, de Jong APH, Scheefhals N, Mertens E, Catsburg LAE et al. 2020. ORANGE: a CRISPR/Cas9-based genome editing toolbox for epitope tagging of endogenous proteins in neurons. PLOS Biol. 18:e3000665
    [Google Scholar]
  126. Willett M, Pollard HJ, Vlasak M, Morley SJ. 2010. Localization of ribosomes and translation initiation factors to talin/β3-integrin-enriched adhesion complexes in spreading and migrating mammalian cells. Biol. Cell 102:265–76
    [Google Scholar]
  127. 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. 178:965–80
    [Google Scholar]
  128. Wong HH, Lin JQ, Strohl F, Roque CG, Cioni JM et al. 2017. RNA docking and local translation regulate site-specific axon remodeling in vivo. Neuron 95:852–68.e8
    [Google Scholar]
  129. Wu B, Eliscovich C, Yoon YJ, Singer RH. 2016. Translation dynamics of single mRNAs in live cells and neurons. Science 352:1430–35
    [Google Scholar]
  130. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A et al. 2005. Local translation of RhoA regulates growth cone collapse. Nature 436:1020–24
    [Google Scholar]
  131. Wu Y, Whiteus C, Xu CS, Hayworth KJ, Weinberg RJ et al. 2017. Contacts between the endoplasmic reticulum and other membranes in neurons. PNAS 114:E4859–67
    [Google Scholar]
  132. Yan X, Hoek TA, Vale RD, Tanenbaum ME 2016. Dynamics of translation of single mRNA molecules in vivo. Cell 165:976–89
    [Google Scholar]
  133. 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. 9:1265–73
    [Google Scholar]
  134. Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE. 2012. Local translation of extranuclear lamin B promotes axon maintenance. Cell 148:752–64
    [Google Scholar]
  135. Younts TJ, Monday HR, Dudok B, Klein ME, Jordan BA et al. 2016. Presynaptic protein synthesis is required for long-term plasticity of GABA release. Neuron 92:479–92
    [Google Scholar]
  136. Yu J, Chen M, Huang H, Zhu J, Song H et al. 2018. Dynamic m6A modification regulates local translation of mRNA in axons. Nucleic Acids Res. 46:1412–23
    [Google Scholar]
  137. Zappulo A, van den Bruck D, Ciolli Mattioli C, Franke V, Imami K et al. 2017. RNA localization is a key determinant of neurite-enriched proteome. Nat. Commun. 8:583
    [Google Scholar]
  138. 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. 30:15464–78
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-083021-110015
Loading
/content/journals/10.1146/annurev-neuro-083021-110015
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error