MiR-124 acts through CoREST to control onset of Sema3A sensitivity in navigating retinal growth cones

Nature Neuroscience

Volumn 15, Issue 1, 2012, Pages 29-38

  Baudet, Marie Laure ^a   Zivraj, Krishna H ^a   Abreu Goodger, Cei ^b   Muldal, Alistair ^a   Armisen, Javier ^c   Blenkiron, Cherie ^c   Goldstein, Leonard D ^c   Miska, Eric A ^c   Holt, Christine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MIR 124; NEUROPILIN 1; REPRESSOR ELEMENT 1 SILENCING TRANSCRIPTION FACTOR COFACTOR; SEMAPHORIN 3A; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EMBRYO; GROWTH CONE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA; RETINA GANGLION CELL; XENOPUS LAEVIS;

ANIMALS; AXONS; CELL DIFFERENTIATION; CELL MOVEMENT; GROWTH CONES; MICRORNAS; NERVE TISSUE PROTEINS; NEUROPILIN-1; REPRESSOR PROTEINS; RETINAL GANGLION CELLS; SEMAPHORIN-3A; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

EID: 84655170104     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2979     Document Type: Article

References (50)

1. Tessier-Lavigne, M. & Goodman, C.S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996). (Pubitemid 26389268)
2. Dickson, B.J. Molecular mechanisms of axon guidance. Science 298, 1959-1964 (2002). (Pubitemid 35425245)
3. Zou, Y., Stoeckli, E., Chen, H. & Tessier-Lavigne, M. Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102, 363-375 (2000).
4. Stein, E. & Tessier-Lavigne, M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291, 1928-1938 (2001). (Pubitemid 32216987)
5. Shewan, D., Dwivedy, A., Anderson, R. & Holt, C.E. Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat. Neurosci. 5, 955-962 (2002).
6. Campbell, D.S. et al. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547 (2001). (Pubitemid 33051452)
7. Piper, M. et al. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49, 215-228 (2006). (Pubitemid 43089639)
8. Shirasaki, R., Katsumata, R. & Murakami, F. Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 279, 105-107 (1998). (Pubitemid 28079166)
9. Johnson, M.H. & Day, M.L. Egg timers: how is developmental time measured in the early vertebrate embryo? Bioessays 22, 57-63 (2000). (Pubitemid 30057134)
10. Aulehla, A. & Pourquié, O. Signaling gradients during paraxial mesoderm development. Cold Spring Harb. Perspect. Biol. 2, a000869 (2010).
11. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862 (1993). (Pubitemid 24014543)
12. Reinhart, B.J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906 (2000). (Pubitemid 30130993)
13. Lee, R.C., Feinbaum, R.L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854 (1993). (Pubitemid 24014542)
14. Decembrini, S. et al. MicroRNAs couple cell fate and developmental timing in retina. Proc. Natl. Acad. Sci. USA 106, 21179-21184 (2009).
15. Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
16. Krichevsky, A.M., King, K.S., Donahue, C.P., Khrapko, K. & Kosik, K.S. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9, 1274-1281 (2003). (Pubitemid 37151681)
17. Wienholds, E. MicroRNA expression in zebrafish embryonic development. Science 309, 310-311 (2005). (Pubitemid 40967869)
18. Moss, E.G. Heterochronic genes and the nature of developmental time. Curr. Biol. 17, R425-R434 (2007). (Pubitemid 46829826)
19. Smirnova, L. et al. Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21, 1469-1477 (2005). (Pubitemid 40646593)
20. Sempere, L.F. et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13 (2004).
21. Holt, C.E. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J. Neurosci. 9, 3123-3145 (1989). (Pubitemid 19260829)
22. Griffiths-Jones, S., Grocock, R.J., Van Dongen, S., Bateman, A. & Enright, A.J. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140-D144 (2006).
23. Kloosterman, W.P., Lagendijk, A.K., Ketting, R.F., Moulton, J.D. & Plasterk, R.H.A. Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 5, e203 (2007).
24. Gao, F.-B. Context-dependent functions of specific microRNAs in neuronal development. Neural Dev. 5, 25 (2010).
25. Taranova, O.V. et al. SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20, 1187-1202 (2006).
26. Hocking, J.C., Hehr, C.L., Bertolesi, G.E., Wu, J.Y. & McFarlane, S. Distinct roles for Robo2 in the regulation of axon and dendrite growth by retinal ganglion cells. Mech. Dev. 127, 36-48 (2010).
27. Visvanathan, J., Lee, S., Lee, B., Lee, J.W. & Lee, S.-K. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 21, 744-749 (2007). (Pubitemid 46572354)
28. Cheng, L.-C., Pastrana, E., Tavazoie, M. & Doetsch, F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12, 399-408 (2009).
29. Clark, A.M. et al. The microRNA miR-124 controls gene expression in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Res. 38, 3780-3793 (2010).
30. Cao, X., Pfaff, S.L. & Gage, F.H. A functional study of miR-124 in the developing neural tube. Genes Dev. 21, 531-536 (2007). (Pubitemid 46409468)
31. Holt, C.E. Does timing of axon outgrowth influence initial retinotectal topography in Xenopus? J. Neurosci. 4, 1130-1152 (1984).
32. Kurschat, P., Bielenberg, D., Rossignol-Tallandier, M., Stahl, A. & Klagsbrun, M. Neuron restrictive silencer factor NRSF/REST is a transcriptional repressor of neuropilin-1 and diminishes the ability of semaphorin 3A to inhibit keratinocyte migration. J. Biol. Chem. 281, 2721-2729 (2006). (Pubitemid 43845735)
33. Diefenbach, T.J., Guthrie, P.B. & Kater, S.B. Stimulus history alters behavioral responses of neuronal growth cones. J. Neurosci. 20, 1484-1494 (2000). (Pubitemid 30220427)
34. Zivraj, K.H. et al. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464-15478 (2010).
35. Giraldez, A.J. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75-79 (2006).
36. Jung, H., O'Hare, C.M. & Holt, C.E. Translational regulation in growth cones. Curr. Opin. Genet. Dev. 21, 458-464 (2011).
37. Leung, K.-M. et al. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247-1256 (2006). (Pubitemid 44454266)
38. Wu, K.Y. et al. Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024 (2005). (Pubitemid 41191685)
39. Keleman, K. et al. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110, 415-427 (2002). (Pubitemid 35232286)
40. Chen, H., He, Z., Bagri, A. & Tessier-Lavigne, M. Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins. Neuron 21, 1283-1290 (1998). (Pubitemid 29022531)
41. Brittis, P.A., Lu, Q. & Flanagan, J.G. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110, 223-235 (2002). (Pubitemid 34876550)
42. Mann, F., Harris, W.A. & Holt, C.E. New views on retinal axon development: a navigation guide. Int. J. Dev. Biol. 48, 957-964 (2004). (Pubitemid 40039185)
43. Atkinson-Leadbeater, K. et al. Dynamic expression of axon guidance cues required for optic tract development is controlled by fibroblast growth factor signaling. J. Neurosci. 30, 685-693 (2010).
44. Feldheim, D.A. et al. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563-574 (2000).
45. Pinter, R. & Hindges, R. Perturbations of microRNA function in mouse dicer mutants produce retinal defects and lead to aberrant axon pathfinding at the optic chiasm. PLoS ONE 5, e10021 (2010).
46. Nieuwkoop, P.D. & Faber, J. Normal Table of Xenopus laevis (Daudin) (Garland, New York and London, 1994).
47. Cornel, E. & Holt, C. Precocious pathfinding: retinal axons can navigate in an axonless brain. Neuron 9, 1001-1011 (1992). (Pubitemid 23007173)
48. Obernosterer, G., Martinez, J. & Alenius, M. Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat. Protoc. 2, 1508-1514 (2007). (Pubitemid 46952329)
49. Falk, J. et al. Electroporation of cDNA/Morpholinos to targeted areas of embryonic CNS in Xenopus. BMC Dev. Biol. 7, 107 (2007).
50. Grimson, A. et al. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (2007). (Pubitemid 46991392)