Insights into the roles of local translation from the axonal transcriptome

Open Biology

Volumn 2, Issue JUNE, 2012, Pages

  Deglincerti, Alessia ^a,b   Jaffrey, Samie R ^b  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Axonal transcriptome; Functions of local mRNA translation; Microarray analysis

Indexed keywords

MESSENGER RNA; NERVE PROTEIN; TRANSCRIPTOME;

ANIMAL; AXONAL TRANSCRIPTOME; BIOSYNTHESIS; FUNCTIONS OF LOCAL MRNA TRANSLATION; HUMAN; METABOLISM; MICROARRAY ANALYSIS; NERVE FIBER; PHYSIOLOGY; PROTEIN SYNTHESIS; REVIEW;

AXONAL TRANSCRIPTOME; FUNCTIONS OF LOCAL MRNA TRANSLATION; MICROARRAY ANALYSIS;

ANIMALS; AXONS; HUMANS; NERVE TISSUE PROTEINS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84864265937     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.120079     Document Type: Article

References (109)

1. 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, 62-79. (doi:10.1016/0006-8993(76)90961-6)
2. Hughes A. 1955 The development of the neural tube of the chick embryo. A study with the ultraviolet microscope. J. Embryol. Exp. Morphol. 3, 305-325.
3. Edstrom JE, Eichner D, Edstrom A. 1962 The ribonucleic acid of axons and myelin sheaths from Mauthner neurons. Biochim. Biophys. Acta 61, 178-184. (doi:10.1016/0926-6550(62)90080-4)
4. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS. 1998 Sorting of b-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251-265. (doi:10.1111/j.1474-919X. 1972.tb02603.x) (Pubitemid 28046786)
5. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL. 2001 A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. 21, 9291-9303. (Pubitemid 33096873)
6. Campbell DS, Holt CE. 2001 Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026. (doi:10.1016/S0896-6273(01)00551-7) (Pubitemid 34075393)
7. Gumy LF et al. 2011 Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17, 85-98. (doi:10.1073/pnas.0801789105)
8. Zivraj KH, Tung YC, Piper M, Gumy L, Fawcett JW, Yeo GS, Holt CE. 2010 Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15 464-15 478. (doi:10.1523/JNEUROSCI. 1800-10.2010)
9. 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, 308-324. (doi:10.1038/nrn3210)
10. Jung H, Holt CE. 2011 Local translation of mRNAs in neural development. Wiley Interdiscip. Rev. RNA 2, 153-165. (doi:10.1002/wrna.53)
11. Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, Urquhart ER, Jaffrey SR. 2005 Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024. (doi:10.1038/nature03885) (Pubitemid 41191685)
12. Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE. 2006 Asymmetrical b-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247-1256. (doi:10.1038/nn1775) (Pubitemid 44454266)
13. Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ. 2006 An essential role for b-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 9, 1265-1273. (doi:10. 1038/nn1773) (Pubitemid 44454268)
14. Zhang HL, Singer RH, Bassell GJ. 1999 Neurotrophin regulation of b-actin mRNA and protein localization within growth cones. J. Cell Biol. 147, 59-70. (doi:10.1083/jcb.147.1.59) (Pubitemid 30211796)
15. Piper M, Anderson R, Dwivedy A, Weinl C, van Horck F, Leung KM, Cogill E, Holt C. 2006 Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49, 215-228. (doi:10.1016/j.neuron.2005.12.008) (Pubitemid 43089639)
16. Hengst U, Deglincerti A, Kim HJ, Jeon NL, Jaffrey SR. 2009 Axonal elongation triggered by stimulusinduced local translation of a polarity complex protein. Nat. Cell Biol. 11, 1024-1030. (doi:10. 1038/ncb1916)
17. van Kesteren RE, Carter C, Dissel HM, van Minnen J, Gouwenberg Y, Syed NI, Spencer GE, Smit AB. 2006 Local synthesis of actin-binding protein beta-thymosin regulates neurite outgrowth. J. Neurosci. 26, 152-157. (doi:10.1523/ JNEUROSCI.4164-05.2006) (Pubitemid 43090916)
18. Natera-Naranjo O, Kar AN, Aschrafi A, Gervasi NM, Macgibeny MA, Gioio AE, Kaplan BB. 2012 Local translation of ATP synthase subunit 9 mRNA alters ATP levels and the production of ROS in the axon. Mol. Cell Neurosci. 49, 263-270. (doi:10.1016/j.mcn.2011.12.006)
19. Aschrafi A, Natera-Naranjo O, Gioio AE, Kaplan BB. 2010 Regulation of axonal trafficking of cytochrome c oxidase IV mRNA. Mol. Cell Neurosci. 43, 422-430. (doi:10.1007/s001140050348)
20. Thelen K, Maier B, Faber M, Albrecht C, Fischer P, Pollerberg GE. 2012 Translation of the cell adhesion molecule ALCAM in axonal growth cones-regulation and functional importance. J. Cell Sci. 125, 1003-1014. (doi:10.1242/jcs.096149)
21. Kundel M, Jones KJ, Shin CY, Wells DG. 2009 Cytoplasmic polyadenylation element-binding protein regulates neurotrophin-3-dependent betacatenin mRNA translation in developing hippocampal neurons. J. Neurosci. 29, 13 630-13 639. (doi:10.1523/JNEUROSCI.2910-08.2009)
22. Andreassi C, Zimmermann C, Mitter R, Fusco S, Devita S, Saiardi A, Riccio A. 2010 An NGFresponsive element targets myo-inositol monophosphatase-1 mRNA to sympathetic neuron axons. Nat. Neurosci. 13, 291-301. (doi:10.1038/ nn.2486)
23. 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, 752-764. (doi:10.1016/j.cell.2011.11.064)
24. 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, 12 581-12 590. (doi:10.1523/JNEUROSCI.3338-08.2008)
25. Akten B et al. 2011 Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc. Natl Acad. Sci. USA 108, 10 337-10 342. (doi:10.1073/ pnas.1104928108)
26. Twiss JL, Smith DS, Chang B, Shooter EM. 2000 Translational control of ribosomal protein L4 mRNA is required for rapid neurite regeneration. Neurobiol. Dis. 7, 416-428. (doi:10.1006/nbdi.2000.0293)
27. Hanz S et al. 2003 Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104. (doi:10.1016/S0896-6273 (03)00770-0) (Pubitemid 38032787)
28. Yudin D et al. 2008 Localized regulation of axonal RanGTPase controls retrograde injury signaling in peripheral nerve. Neuron 59, 241-252. (doi:10. 1016/j.neuron.2008.05.029) (Pubitemid 352033684)
29. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, Fainzilber M. 2005 Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45, 715-726. (doi:10. 1016/j.neuron.2005.01.023) (Pubitemid 40320706)
30. Sotelo-Silveira JR, Calliari A, Kun A, Benech JC, Sanguinetti C, Chalar C, Sotelo JR. 2000 Neurofilament mRNAs are present and translated in the normal and severed sciatic nerve. J. Neurosci. Res. 62, 65-74. (doi:10.1002/1097- 4547(20001001)62:1, 65::AID-JNR7.3.0.CO;2-Z)
31. 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, 149-159. (doi:10.1038/ncb1677) (Pubitemid 351194044)
32. Ben-Yaakov K et al. 2012 Axonal transcription factors signal retrogradely in lesioned peripheral nerve. EMBO J. 31, 1350-1363. (doi:10.1038/emboj.2011. 494)
33. Ji SJ, Jaffrey SR. 2012 Intra-axonal translation of SMAD1/5/8 mediates retrograde regulation of trigeminal ganglia subtype specification. Neuron 74, 95-107. (doi:10.1016/j.neuron.2012.02.022)
34. Yan D, Wu Z, Chisholm AD, Jin Y. 2009 The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138, 1005-1018. (doi:10.1016/ j.cell.2009.06.023)
35. Moccia R et al. 2003 An unbiased cDNA library prepared from isolated Aplysia sensory neuron processes is enriched for cytoskeletal and translational mRNAs. J. Neurosci. 23, 9409-9417. (Pubitemid 37323041)
36. Lyles V, Zhao Y, Martin KC. 2006 Synapse formation and mRNA localization in cultured Aplysia neurons. Neuron 49, 349-356. (doi:10.1016/j.neuron.2005. 12.029) (Pubitemid 43152237)
37. Dubacq C, Jamet S, Trembleau A. 2009 Evidence for developmentally regulated local translation of odorant receptor mRNAs in the axons of olfactory sensory neurons. J. Neurosci. 29, 10 184-10 190. (doi:10.1523/JNEUROSCI.2443-09. 2009)
38. Bi J, Tsai NP, Lin YP, Loh HH, Wei LN. 2006 Axonal mRNA transport and localized translational regulation of kappa-opioid receptor in primary neurons of dorsal root ganglia. Proc. Natl Acad. Sci. USA 103, 19 919-19 924. (doi:10.1073/pnas. 0607394104) (Pubitemid 46037531)
39. Ming GL, Wong ST, Henley J, Yuan XB, Song HJ, Spitzer NC, Poo MM. 2002 Adaptation in the chemotactic guidance of nerve growth cones. Nature 417, 411-418. (doi:10.1038/nature745) (Pubitemid 34563528)
40. Hengst U, Cox LJ, Macosko EZ, Jaffrey SR. 2006 Functional and selective RNA interference in developing axons and growth cones. J. Neurosci. 26, 5727-5732. (doi:10.1523/JNEUROSCI.5229-05.2006) (Pubitemid 44315264)
41. Mohr E, Fehr S, Richter D. 1991 Axonal transport of neuropeptide encoding mRNAs within the hypothalamo-hypophyseal tract of rats. EMBO J. 10, 2419-2424. (Pubitemid 21905715)
42. 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, 113-125. (doi:10.1016/0306-4522(95)00328-G) (Pubitemid 126755229)
43. Jirikowski GF, Sanna PP, Bloom FE. 1990 mRNA coding for oxytocin is present in axons of the hypothalamo-neurohypophysial tract. Proc. Natl Acad. Sci. USA 87, 7400-7404. (doi:10.1073/pnas. 87.19.7400)
44. Ressler KJ, Sullivan SL, Buck LB. 1994 Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79, 1245-1255. (doi:10. 1016/0092-8674(94)90015-9)
45. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994 Topographic organization of sensory projections to the olfactory bulb. Cell 79, 981-991. (doi:10.1016/0092-8674(94)90029-9)
46. Brittis PA, Lu Q, Flanagan JG. 2002 Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110, 223-235. (doi:10.1016/S0092-8674(02)00813-9) (Pubitemid 34876550)
47. Weiner OD, Zorn AM, Krieg PA, Bittner GD. 1996 Medium weight neurofilament mRNA in goldfish Mauthner axoplasm. Neurosci. Lett. 213, 83-86. (doi:10.1016/0304-3940(96)12860-3) (Pubitemid 26252830)
48. Ressler KJ, Sullivan SL, Buck LB. 1994 A molecular dissection of spatial patterning in the olfactory system. Curr. Opin. Neurobiol. 4, 588-596. (doi:10.1016/0959-4388(94)90061-2) (Pubitemid 24258920)
49. Bassell GJ, Singer RH, Kosik KS. 1994 Association of poly(A) mRNA with microtubules in cultured neurons. Neuron 12, 571-582. (doi:10.1016/0896-6273(94) 90213-5) (Pubitemid 24100888)
50. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW. 2005 Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 25, 331-342. (doi:10.1523/JNEUROSCI.3073-04. 2005) (Pubitemid 40105603)
51. Gioio AE, Eyman M, Zhang H, Lavina ZS, Giuditta A, Kaplan BB. 2001 Local synthesis of nuclear-encoded mitochondrial proteins in the presynaptic nerve terminal. J. Neurosci. Res. 64, 447-453. (doi:10. 1002/jnr.1096) (Pubitemid 32521764)
52. Gioio AE, Lavina ZS, Jurkovicova D, Zhang H, Eyman M, Giuditta A, Kaplan BB. 2004 Nerve terminals of squid photoreceptor neurons contain a heterogeneous population of mRNAs and translate a transfected reporter mRNA. Eur. J. Neurosci. 20, 865-872. (doi:10.1111/j.1460-9568.2004.03538.x) (Pubitemid 39141294)
53. Willis DE et al. 2007 Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol. 178, 965-980. (doi:10.1083/ jcb.200703209) (Pubitemid 47443320)
54. Taylor AM, Berchtold NC, Perreau VM, Tu CH, Li Jeon N, Cotman CW. 2009 Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29, 4697-4707. (doi:10.1523/ JNEUROSCI.6130-08.2009)
55. Wang SM. 2007 Understanding SAGE data. Trends Genet. 23, 42-50. (doi:10.1016/j.tig.2006. 11.001) (Pubitemid 44960529)
56. Havik B, Rokke H, Bardsen K, Davanger S, Bramham CR. 2003 Bursts of high-frequency stimulation trigger rapid delivery of pre-existing alpha-CaMKII mRNA to synapses: a mechanism in dendritic protein synthesis during long-term potentiation in adult awake rats. Eur. J. Neurosci. 17, 2679-2689. (doi:10.1046/j.1460-9568.2003.02712.x) (Pubitemid 36819293)
57. Wang DO, Kim SM, Zhao Y, Hwang H, Miura SK, Sossin WS, Martin KC. 2009 Synapse-and stimulusspecific local translation during long-term neuronal plasticity. Science 324, 1536-1540. (doi:10.1126/ science.1173205)
58. Van Ness J, Maxwell IH, Hahn WE. 1979 Complex population of nonpolyadenylated messenger RNA in mouse brain. Cell 18, 1341-1349. (doi:10.1016/ 0092-8674(79)90244-7) (Pubitemid 10172711)
59. Snider BJ, Morrison-Bogorad M. 1992 Brain non-adenylated mRNAs. Brain Res. Brain Res. Rev. 17, 263-282. (doi:10.1016/0165-0173(92) 90019-I)
60. Lin AC, Tan CL, Lin CL, Strochlic L, Huang YS, Richter JD, Holt CE. 2009 Cytoplasmic polyadenylation and cytoplasmic polyadenylation element-dependent mRNA regulation are involved in Xenopus retinal axon development. Neural Dev. 4, 8. (doi:10. 1186/1749-8104-4-8)
61. Bassell G, Singer RH. 1997 mRNA and cytoskeletal filaments. Curr. Opin. Cell Biol. 9, 109-115. (doi:10. 1016/S0955-0674(97)80159-7) (Pubitemid 27065116)
62. Kiebler MA, Bassell GJ. 2006 Neuronal RNA granules: movers and makers. Neuron 51, 685-690 (doi:10.1016/j.neuron.2006.08.021) (Pubitemid 44374907)
63. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG. 2010 Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141, 632-644. (doi:10. 1016/j.cell.2010.04.008)
64. Krichevsky AM, Kosik KS. 2001 Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32, 683-696. (doi:10.1016/S0896-6273(01)00508-6) (Pubitemid 33145201)
65. Bellamy D. 1962 The endogenous citric acid-cycle intermediates and amino acids of mitochondria. Biochem. J. 82, 218-224.
66. Goffart S, Wiesner RJ. 2003 Regulation and coordination of nuclear gene expression during mitochondrial biogenesis. Exp. Physiol. 88, 33-40. (doi:10.1113/eph8802500) (Pubitemid 36150057)
67. Anderson S et al. 1981 Sequence and organization of the human mitochondrial genome. Nature 290, 457-465. (doi:10.1038/290457a0) (Pubitemid 11159074)
68. Neupert W, Herrmann JM. 2007 Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749. (doi:10.1146/annurev.biochem.76. 052705.163409)
69. 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, 701-716. (doi:10.1007/s10571-007-9148-y) (Pubitemid 47485283)
70. Korostelev AA. 2011 Structural aspects of translation termination on the ribosome. RNA 17, 1409-1421. (doi:10.1261/rna.2733411)
71. Strunk BS, Karbstein K. 2009 Powering through ribosome assembly. RNA 15, 2083-2104. (doi:10. 1261/rna.1792109)
72. Knowles RB, Sabry JH, Martone ME, Deerinck TJ, Ellisman MH, Bassell GJ, Kosik KS. 1996 Translocation of RNA granules in living neurons. J. Neurosci. 16, 7812-7820. (Pubitemid 26405044)
73. Kraft C, Deplazes A, Sohrmann M, Peter M. 2008 Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 10, 602-610. (doi:10.1038/ncb1723) (Pubitemid 351627380)
74. Gilbert WV. 2011 Functional specialization of ribosomes? Trends Biochem. Sci. 36, 127-132. (doi:10.1016/j.tibs.2010.12.002)
75. Chook YM, Blobel G. 2001 Karyopherins and nuclear import. Curr. Opin. Struct. Biol. 11, 703-715. (doi:10.1016/S0959-440X(01)00264-0) (Pubitemid 34076632)
76. Bi J, Hu X, Loh HH, Wei LN. 2003 Mouse kappaopioid receptor mRNA differential transport in neurons. Mol. Pharmacol. 64, 594-599. (doi:10. 1124/mol.64.3.594) (Pubitemid 37048562)
77. Rapoport TA. 2007 Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669. (doi:10.1038/nature06384) (Pubitemid 350207698)
78. Pfeffer SR, Rothman JE. 1987 Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annu. Rev. Biochem. 56, 829-852. (doi:10.1146/annurev.bi.56.070187.004145)
79. Tsukita S, Ishikawa H. 1976 Three-dimensional distribution of smooth endoplasmic reticulum in myelinated axons. J. Electron Microsc. (Tokyo) 25, 141-149. (Pubitemid 8067997)
80. Merianda TT, Lin AC, Lam JS, Vuppalanchi D, Willis DE, Karin N, Holt CE, Twiss JL. 2009 A functional equivalent of endoplasmic reticulum and Golgi in axons for secretion of locally synthesized proteins. Mol. Cell Neurosci. 40, 128-142. (doi:10.1016/j. mcn.2008.09.008)
81. Horton AC, Ehlers MD. 2003 Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23, 6188-6199. (Pubitemid 36875619)
82. Pelletier L, Jokitalo E, Warren G. 2000 The effect of Golgi depletion on exocytic transport. Nat. Cell Biol. 2, 840-846. (doi:10.1038/35041089)
83. Segal RA. 2003 Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci. 26, 299-330 (doi:10.1146/annurev.neuro.26. 041002.131421) (Pubitemid 37064936)
84. Butowt R, von Bartheld CS. 2001 Sorting of internalized neurotrophins into an endocytic transcytosis pathway via the Golgi system: ultrastructural analysis in retinal ganglion cells. J. Neurosci. 21, 8915-8930. (Pubitemid 33054854)
85. Donnelly CJ et al. 2011 Limited availability of ZBP1 restricts axonal mRNA localization and nerve regeneration capacity. EMBO J. 30, 4665-4677. (doi:10.1038/emboj.2011.347)
86. Willis DE et al. 2011 Axonal localization of transgene mRNA in mature PNS and CNS neurons. J. Neurosci. 31, 14 481-14 487. (doi:10.1523/ JNEUROSCI.2950-11.2011)
87. Heiman M et al. 2008 A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748. (doi:10.1016/j.cell. 2008.10.028)
88. Walker BA, Hengst U, Kim HJ, Jeon NL, Schmidt EF, Heintz N, Milner TA, Jaffrey SR. In press. Reprogramming axonal behavior by axon-specific viral transduction. Gene Ther. (doi:10.1038/gt.2011.217)
89. Doyle JP et al. 2008 Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749-762. (doi:10.1016/j. cell.2008.10.028)
90. Court FA, Hendriks WT, Macgillavry HD, Alvarez J, van Minnen J. 2008 Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J. Neurosci. 28, 11 024-11 029. (doi:10.1523/ JNEUROSCI.2429-08.2008)
91. Jeromin A, Yuan LL, Frick A, Pfaffinger P, Johnston D. 2003 A modified Sindbis vector for prolonged gene expression in neurons. J. Neurophysiol. 90, 2741-2745. (doi:10.1152/jn.00464.2003) (Pubitemid 37266538)
92. Agard NJ, Prescher JA, Bertozzi CR. 2004 A strainpromoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126, 15 046-15 047. (doi:10.1021/ja044996f ) (Pubitemid 39557262)
93. Tian B, Hu J, Zhang H, Lutz CS. 2005 A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res. 33, 201-212. (doi:10.1093/nar/gki158) (Pubitemid 40276942)
94. Wang Z, Gerstein M, Snyder M. 2009 RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63. (doi:10.1038/nrg2484)
95. Natera-Naranjo O, Aschrafi A, Gioio AE, Kaplan BB. 2010 Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. RNA 16, 1516-1529. (doi:10.1261/rna.1833310)
96. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N. 2012 microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat. Neurosci. 15, 697-699. (doi:10.1038/nn.3082)
97. Kislauskis EH, Zhu X, Singer RH. 1994 Sequences responsible for intracellular localization of b-actin messenger RNA also affect cell phenotype. J. Cell Biol. 127, 441-451. (doi:10. 1083/jcb.127.2.441) (Pubitemid 24313732)
98. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ. 2001 Neurotrophin-induced transport of a b-actin mRNP complex increases b-actin levels and stimulates growth cone motility. Neuron 31, 261-275. (doi:10.1016/S0896-6273(01)00357-9) (Pubitemid 32762979)
99. Patel VL et al. 2012 Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control. Genes Dev. 26, 43-53. (doi:10.1101/gad. 177428.111)
100. Welshhans K, Bassell GJ. 2011 Netrin-1-induced local b-actin synthesis and growth cone guidance requires zipcode binding protein 1. J. Neurosci. 31, 9800-9813. (doi:10.1523/JNEUROSCI.0166-11. 2011)
101. Meyuhas O. 2000 Synthesis of the translational apparatus is regulated at the translational level. Eur. J. Biochem. 267, 6321-6330. (doi:10.1046/j. 1432-1327.2000.01719.x)
102. Iadevaia V, Caldarola S, Tino E, Amaldi F, Loreni F. 2008 All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 50-terminal oligopyrimidine (TOP) mRNAs. RNA 14, 1730-1736. (doi:10.1261/rna. 1037108)
103. Pellizzoni L, Lotti F, Maras B, Pierandrei-Amaldi P. 1997 Cellular nucleic acid binding protein binds a conserved region of the 50 UTR of Xenopus laevis ribosomal protein mRNAs. J. Mol. Biol. 267, 264-275. (doi:10.1006/jmbi. 1996.0888) (Pubitemid 27149839)
104. van Niekerk EA, Willis DE, Chang JH, Reumann K, Heise T, Twiss JL. 2007 Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc. Natl Acad. Sci. USA 104, 12 913-12 918. (doi:10.1073/pnas.0611562104) (Pubitemid 47255254)
105. Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinski M, Jacq C. 2002 Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3, 159-164. (doi:10.1093/emboreports/ kvf025) (Pubitemid 34213494)
106. Sylvestre J, Vialette S, Corral Debrinski M, Jacq C. 2003 Long mRNAs coding for yeast mitochondrial proteins of prokaryotic origin preferentially localize to the vicinity of mitochondria. Genome Biol. 4, R44. (doi:10.1186/gb-2003-4-7-r44)
107. Eliyahu E, Pnueli L, Melamed D, Scherrer T, Gerber AP, Pines O, Rapaport D, Arava Y. 2010 Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner. Mol. Cell Biol. 30, 284-294. (doi:10.1128/MCB. 00651-09)
108. Lee SK, Hollenbeck PJ. 2003 Organization and translation of mRNA in sympathetic axons. J. Cell Sci. 116, 4467-4478. (doi:10.1242/jcs.00745) (Pubitemid 37369601)
109. Eng H, Lund K, Campenot RB. 1999 Synthesis of beta-tubulin, actin, and other proteins in axons of sympathetic neurons in compartmented cultures. J. Neurosci. 19, 1-9. (Pubitemid 29028943)