Local translation and directional steering in axons

EMBO Journal

Volumn 26, Issue 16, 2007, Pages 3729-3736

  Lin, Andrew C ^a   Holt, Christine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Axon guidance; Growth cone; RNA binding protein; Translation

Indexed keywords

BETA ACTIN; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; PROTEIN; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; CALCIUM TRANSPORT; CELL MIGRATION; CELL POLARITY; DROSOPHILA; GROWTH CONE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA INTERFERENCE; RNA SPLICING; RNA TRANSLATION; TRANSLATION INITIATION; XENOPUS;

ANIMALS; AXONS; BRAIN; CELL MOVEMENT; GENE EXPRESSION REGULATION; GROWTH CONES; NEURONAL PLASTICITY; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EID: 34548056140     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601808     Document Type: Review

References (98)

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
2. Anderson P, Kedersha N (2006) RNA granules. J Cell Biol 172: 803-808
3. Antar LN, Li C, Zhang H, Carroll RC, Bassell GJ (2006) Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. Mol Cell Neurosci 32: 37-48
4. Aronov S, Aranda G, Behar L, Ginzburg I (2001) Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal. J Neurosci 21: 6577-6587
5. Ashraf SI, McLoon AL, Sclarsic SM, Kunes S (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124: 191-205
6. Atkins CM, Nozaki N, Shigeri Y, Soderling TR (2004) Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J Neurosci 24: 5193-5201
7. 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 26: 9743-9749
8. Blackmore M, Letourneau PC (2007) Protein synthesis in distal axons is not required for axon growth in the embryonic spinal cord. Dev Neurobiol 67: 976-986
9. Brittis PA, Lu Q, Flanagan JG (2002) Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110: 223-235
10. Brunet I, Weinl C, Piper M, Trembleau A, Volovitch M, Harris W, Prochiantz A, Holt C (2005) The transcription factor Engrailed-2 guides retinal axons. Nature 438: 94-98
11. Bunge MB (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture. J Cell Biol 56: 713-735
12. Caceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343: 461-463
13. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32: 1013-1026
14. Campbell DS, Holt CE (2003) Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37: 939-952
15. Cao Q, Kim JH, Richter JD (2006) CDK1 and calcineurin regulate Maskin association with eIF4E and translational control of cell cycle progression. Nat Struct Mol Biol 13: 1128-1134
16. Chihara T, Luginbuhl D, Luo L (2007) Cytoplasmic and mitochondrial protein translation in axonal and dendritic terminal arborization. Nat Neurosci 10: 828-837
17. Condeelis J, Singer RH (2005) How and why does beta-actin mRNA target? Biol Cell 97: 97-110
18. Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, Fratto CM, Tolley E, Kraiss LW, McIntyre TM, Zimmerman GA, Weyrich AS (2005) Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 122: 379-391
19. dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, Berry DA, Nosworthy NJ (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 83: 433-473
20. Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26: 597-604
21. 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
22. Fonseca R, Nagerl UV, Bonhoeffer T (2006) Neuronal activity determines the protein synthesis dependence of long-term potentiation. Nat Neurosci 9: 478-480
23. Gebauer F, Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835
24. 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: 400-404
25. Glanzer J, Miyashiro KY, Sul JY, Barrett L, Belt B, Haydon P, Eberwine J (2005) RNA splicing capability of live neuronal dendrites. Proc Natl Acad Sci USA 102: 16859-16864
26. Gomez TM, Zheng JQ (2006) The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 7: 115-125
27. Grantham J, Ruddock LW, Roobol A, Carden MJ (2002) Eukaryotic chaperonin containing T-complex polypeptide 1 interacts with filamentous actin and reduces the initial rate of actin polymerization in vitro. Cell Stress Chaperones 7: 235-242
28. Grossman AW, Aldridge GM, Weiler IJ, Greenough WT (2006) Local protein synthesis and spine morphogenesis: Fragile X syndrome and beyond. J Neurosci 26: 7151-7155
29. Guirland C, Buck KB, Gibney JA, DiCicco-Bloom E, Zheng JQ (2003) Direct cAMP signaling through G-protein-coupled receptors mediates growth cone attraction induced by pituitary adenylate cyclase-activating polypeptide. J Neurosci 23: 2274-2283
30. Hansen WJ, Cowan NJ, Welch WJ (1999) Prefoldin-nascent chain complexes in the folding of cytoskeletal proteins. J Cell Biol 145: 265-277
31. 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: 123-133
32. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858
33. 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
34. Henley J, Poo MM (2004) Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 14: 320-330
35. Henley JR, Huang KH, Wang D, Poo MM (2004) Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron 44: 909-916
36. Hong K, Nishiyama M, Henley J, Tessier-Lavigne M, Poo M (2000) Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403: 93-98
37. 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
38. Hu JY, Goldman J, Wu F, Schacher S (2004) Target-dependent release of a presynaptic neuropeptide regulates the formation and maturation of specific synapses in Aplysia. J Neurosci 24: 9933-9943
39. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, Bassell GJ, Condeelis J, Singer RH (2005) Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 438: 512-515
40. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117: 5721-5729
41. Johnstone O, Lasko P (2001) Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu Rev Genet 35: 365-406
42. Karakozova M, Kozak M, Wong CC, Bailey AO, Yates III JR, Mogilner A, Zebroski H, Kashina A (2006) Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science 313: 192-196
43. Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51: 685-690
44. Kislauskis EH, Zhu X, Singer RH (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J Cell Biol 127: 441-451
45. Klann E, Dever TE (2004) Biochemical mechanisms for translational regulation in synaptic plasticity. Nat Rev Neurosci 5: 931-942
46. Koenig E, Giuditta A (1999) Protein-synthesizing machinery in the axon compartment. Neuroscience 89: 5-15
47. Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32: 683-696
48. Lee S, Nahm M, Lee M, Kwon M, Kim E, Zadeh AD, Cao H, Kim HJ, Lee ZH, Oh SB, Yim J, Kolodziej PA, Lee S (2007) The F-actin-microtubule crosslinker Shot is a platform for Krasavietz-mediated translational regulation of midline axon repulsion. Development 134: 1767-1777
49. Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE (2006) Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat Neurosci 9: 1247-1256
50. Lisman JE, Zhabotinsky AM (2001) A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31: 191-201
51. Lujan HD, Marotta A, Mowatt MR, Sciaky N, Lippincott-Schwartz J, Nash TE (1995) Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem 270: 4612-4618
52. Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1: 173-180
53. Lyles V, Zhao Y, Martin KC (2006) Synapse formation and mRNA localization in cultured Aplysia neurons. Neuron 49: 349-356
54. 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: 323-336
55. 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
56. Ooashi N, Futatsugi A, Yoshihara F, Mikoshiba K, Kamiguchi H (2005) Cell adhesion molecules regulate Ca2+-mediated steering of growth cones via cyclic AMP and ryanodine receptor type 3. J Cell Biol 170: 1159-1167
57. Pappenberger G, McCormack EA, Willison KR (2006) Quantitative actin folding reactions using yeast CCT purified via an internal tag in the CCT3/gamma subunit. J Mol Biol 360: 484-496
58. Perrone-Bizzozero N, Bolognani F (2002) Role of HuD and other RNA-binding proteins in neural development and plasticity. J Neurosci Res 68: 121-126
59. Pinkstaff JK, Chappell SA, Mauro VP, Edelman GM, Krushel LA (2001) Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc Natl Acad Sci USA 98: 2770-2775
60. 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
61. Piper M, Holt C (2004) RNA translation in axons. Annu Rev Cell Dev Biol 20: 505-523
62. 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: 179-186
63. Raab-Graham KF, Haddick PC, Jan YN, Jan LY (2006) Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314: 144-148
64. Richter JD (2007) CPEB: a life in translation. Trends Biochem Sci 32: 279-285
65. Rodriguez AJ, Shenoy SM, Singer RH, Condeelis J (2006) Visualization of mRNA translation in living cells. J Cell Biol 175: 67-76
66. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH (1997) Characterization of a beta-actin mRNA zipcode-binding protein. Mol Cell Biol 17: 2158-2165
67. Schmidt JT (2004) Activity-driven sharpening of the retinotectal projection: the search for retrograde synaptic signaling pathways. J Neurobiol 59: 114-133
68. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439: 283-289
69. Shestakova EA, Singer RH, Condeelis J (2001) The physiological significance of beta -actin mRNA localization in determining cell polarity and directional motility. Proc Natl Acad Sci USA 98: 7045-7050
70. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281: 1515-1518
71. Sossin WS, DesGroseillers L (2006) Intracellular trafficking of RNA in neurons. Traffic 7: 1581-1589
72. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC, Schuman EM (2006) Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125: 785-799
73. Sutton MA, Schuman EM (2005) Local translational control in dendrites and its role in long-term synaptic plasticity. J Neurobiol 64: 116-131
74. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2: 599-605
75. 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
76. Tojima T, Akiyama H, Itofusa R, Li Y, Katayama H, Miyawaki A, Kamiguchi H (2007) Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat Neurosci 10: 58-66
77. Tsai NP, Bi J, Loh HH, Wei LN (2006) Netrin-1 signaling regulates de novo protein synthesis of kappa opioid receptor by facilitating polysomal partition of its mRNA. J Neurosci 26: 9743-9749
78. Tsai NP, Bi J, Wei LN (2007) The adaptor Grb7 links netrin-1 signaling to regulation of mRNA translation. EMBO J 26: 1522-1531
79. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25: 5833-5843
80. Twiss JL, van Minnen J (2006) New insights into neuronal regeneration: the role of axonal protein synthesis in pathfinding and axonal extension. J Neurotrauma 23: 295-308
81. Ule J, Darnell RB (2006) RNA binding proteins and the regulation of neuronal synaptic plasticity. Curr Opin Neurobiol 16: 102-110
82. 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
83. 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
84. Wang J, Boja ES, Tan W, Tekle E, Fales HM, English S, Mieyal JJ, Chock PB (2001) Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem 276: 47763-47766
85. Wen Z, Guirland C, Ming GL, Zheng JQ (2004) A CaMKII/calcineurin switch controls the direction of Ca(2+)-dependent growth cone guidance. Neuron 43: 835-846
86. Willis D, Li KW, Zheng JQ, Chang JH, Smit A, Kelly T, Merianda TT, Sylvester J, van Minnen J, Twiss JL (2005) Differential transport and local translation of cytoskeletal, injury-response, and neuro-degeneration protein mRNAs in axons. J Neurosci 25: 778-791
87. Willis DE, Twiss JL (2006) The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 16: 111-118
88. 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
89. Yamada KM, Spooner BS, Wessells NK (1971) Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol 49: 614-635
90. Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ (2006) An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat Neurosci 9: 1265-1273
91. Yin HH, Davis MI, Ronesi JA, Lovinger DM (2006) The role of protein synthesis in striatal long-term depression. J Neurosci 26: 11811-11820
92. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, Duan S (2003) Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5: 38-45
93. Zalfa F, Achsel T, Bagni C (2006) mRNPs, polysomes or granules: FMRP in neuronal protein synthesis. Curr Opin Neurobiol 16: 265-269
94. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ (2001) Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31: 261-275
95. Zhang HL, Singer RH, Bassell GJ (1999) Neurotrophin regulation of beta-actin mRNA and protein localization within growth cones. J Cell Biol 147: 59-70
96. Zhang X, Poo MM (2002) Localized synaptic potentiation by BDNF requires local protein synthesis in the developing axon. Neuron 36: 675-688
97. Zheng JQ (2000) Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403: 89-93
98. 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