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Molecular Brain
Published in: Molecular Brain 1/2011

Open Access 01-12-2011 | Research

Regulation of chemotropic guidance of nerve growth cones by microRNA

Authors: Liang Han, Zhexing Wen, Rachel C Lynn, Marie-Laure Baudet, Christine E Holt, Yukio Sasaki, Gary J Bassell, James Q Zheng

Published in: Molecular Brain | Issue 1/2011

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Abstract

Background

The small non-coding microRNAs play an important role in development by regulating protein translation, but their involvement in axon guidance is unknown. Here, we investigated the role of microRNA-134 (miR-134) in chemotropic guidance of nerve growth cones.

Results

We found that miR-134 is highly expressed in the neural tube of Xenopus embryos. Fluorescent in situ hybridization also showed that miR-134 is enriched in the growth cones of Xenopus spinal neurons in culture. Importantly, overexpression of miR-134 mimics or antisense inhibitors blocked protein synthesis (PS)-dependent attractive responses of Xenopus growth cones to a gradient of brain-derived neurotrophic factor (BDNF). However, miR-134 mimics or inhibitors had no effect on PS-independent bidirectional responses of Xenopus growth cones to bone morphogenic protein 7 (BMP7). Our data further showed that Xenopus LIM kinase 1 (Xlimk1) mRNA is a potential target of miR-134 regulation.

Conclusions

These findings demonstrate a role for miR-134 in translation-dependent guidance of nerve growth cones. Different guidance cues may act through distinct signaling pathways to elicit PS-dependent and -independent mechanisms to steer growth cones in response to a wide array of spatiotemporal cues during development.
Appendix
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Literature
1.
Tessier-Lavigne M, Goodman CS: The molecular biology of axon guidance. Science. 1996, 274: 1123-1133. 10.1126/science.274.5290.1123.CrossRefPubMed
2.
Dickson BJ: Molecular mechanisms of axon guidance. Science. 2002, 298: 1959-1964. 10.1126/science.1072165.CrossRefPubMed
3.
Tessier-Lavigne M, Goodman CS: The Molecular Biology of Axon Guidance. Science. 1996, 274: 1123-1133. 10.1126/science.274.5290.1123.CrossRefPubMed
4.
Leung KM, van Horck FP, Lin AC, Allison R, Standart N, Holt CE: Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat Neurosci. 2006, 9: 1247-1256. 10.1038/nn1775.PubMedCentralCrossRefPubMed
5.
Wu KY, Hengst U, Cox LJ, Macosko EZ, Jeromin A, Urquhart ER, Jaffrey SR: Local translation of RhoA regulates growth cone collapse. Nature. 2005, 436: 1020-1024. 10.1038/nature03885.PubMedCentralCrossRefPubMed
6.
Piper M, Anderson R, Dwivedy A, Weinl C, van Horck F, Leung KM, Cogill E, Holt C: Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron. 2006, 49: 215-228. 10.1016/j.neuron.2005.12.008.PubMedCentralCrossRefPubMed
7.
8.
Yao J, Sasaki Y, Wen Z, Bassell GJ, Zheng JQ: An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat Neurosci. 2006, 9: 1265-1273. 10.1038/nn1773.CrossRefPubMed
9.
Campbell DS, Holt CE: Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron. 2001, 32: 1013-1026. 10.1016/S0896-6273(01)00551-7.CrossRefPubMed
10.
Takei N, Inamura N, Kawamura M, Namba H, Hara K, Yonezawa K, Nawa H: Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci. 2004, 24: 9760-9769. 10.1523/JNEUROSCI.1427-04.2004.CrossRefPubMed
11.
Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME: BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci. 2004, 24: 7366-7377. 10.1523/JNEUROSCI.1739-04.2004.CrossRefPubMed
12.
13.
Filipowicz W, Bhattacharyya SN, Sonenberg N: Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat Rev Genet. 2008, 9: 102-114.CrossRefPubMed
14.
15.
Fineberg SK, Kosik KS, Davidson BL: MicroRNAs potentiate neural development. Neuron. 2009, 64: 303-309. 10.1016/j.neuron.2009.10.020.CrossRefPubMed
16.
Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME: A brain-specific microRNA regulates dendritic spine development. Nature. 2006, 439: 283-289. 10.1038/nature04367.CrossRefPubMed
17.
Tamura M, Tamura N, Ikeda T, Koyama R, Ikegaya Y, Matsuki N, Yamada MK: Influence of brain-derived neurotrophic factor on pathfinding of dentate granule cell axons, the hippocampal mossy fibers. Mol Brain. 2009, 2: 2-10.1186/1756-6606-2-2.PubMedCentralCrossRefPubMed
18.
Song HJ, Ming GL, Poo MM: cAMP-Induced Switching in Turning Direction of Nerve Growth Cones. Nature. 1997, 388: 275-279. 10.1038/40864.CrossRefPubMed
19.
Ming GL, Lohof AM, Zheng JQ: Acute Morphogenic and Chemotropic Effects of Neurotrophins On Cultured Embryonic Xenopus Spinal Neurons. Journal of Neuroscience. 1997, 17: 7860-7871.PubMed
20.
Butler SJ, Dodd J: A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons. Neuron. 2003, 38: 389-401. 10.1016/S0896-6273(03)00254-X.CrossRefPubMed
21.
Wen Z, Han L, Bamburg JR, Shim S, Ming GL, Zheng JQ: BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. Journal of Cell Biology. 2007, 178: 107-119. 10.1083/jcb.200703055.PubMedCentralCrossRefPubMed
22.
Wen Z, Han L, Bamburg JR, Shim S, Ming GL, Zheng JQ: BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J Cell Biol. 2007, 178: 107-119. 10.1083/jcb.200703055.PubMedCentralCrossRefPubMed
23.
Nuovo GJ: In situ detection of precursor and mature microRNAs in paraffin embedded, formalin fixed tissues and cell preparations. Methods. 2008, 44: 39-46. 10.1016/j.ymeth.2007.10.008.CrossRefPubMed
24.
Reynisson E, Josefsen MH, Krause M, Hoorfar J: Evaluation of probe chemistries and platforms to improve the detection limit of real-time PCR. J Microbiol Methods. 2006, 66: 206-216. 10.1016/j.mimet.2005.11.006.CrossRefPubMed
25.
Pak CW, Flynn KC, Bamburg JR: Actin-binding proteins take the reins in growth cones. Nat Rev Neurosci. 2008, 9: 136-147. 10.1038/nrn2236.CrossRefPubMed
26.
Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al: A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007, 129: 1401-1414. 10.1016/j.cell.2007.04.040.PubMedCentralCrossRefPubMed
27.
Moon MS, Gomez TM: Adjacent pioneer commissural interneuron growth cones switch from contact avoidance to axon fasciculation after midline crossing. Dev Biol. 2005, 288: 474-486. 10.1016/j.ydbio.2005.09.049.CrossRefPubMed
28.
Shim S, Goh EL, Ge S, Sailor K, Yuan JP, Roderick HL, Bootman MD, Worley PF, Song H, Ming GL: XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat Neurosci. 2005, 8: 730-735. 10.1038/nn1459.PubMedCentralCrossRefPubMed
29.
Hengst U, Cox LJ, Macosko EZ, Jaffrey SR: Functional and selective RNA interference in developing axons and growth cones. Journal of Neuroscience. 2006, 26: 5727-5732. 10.1523/JNEUROSCI.5229-05.2006.CrossRefPubMed
30.
Meister G, Landthaler M, Dorsett Y, Tuschl T: Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA. 2004, 10: 544-550. 10.1261/rna.5235104.PubMedCentralCrossRefPubMed
31.
32.
Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M: Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007, 449: 919-922. 10.1038/nature06205.PubMedCentralCrossRefPubMed
33.
Guirland C, Suzuki S, Kojima M, Lu B, Zheng JQ: Lipid rafts mediate chemotropic guidance of nerve growth cones. Neuron. 2004, 42: 51-62. 10.1016/S0896-6273(04)00157-6.CrossRefPubMed
34.
Huang EJ, Reichardt LF: Neurotrophins: roles in neuronal development and function. Annual Review of Neuroscience. 2001, 24: 677-736. 10.1146/annurev.neuro.24.1.677.PubMedCentralCrossRefPubMed
35.
Zheng JQ, Felder M, Connor JA, Poo MM: Turning of nerve growth cones induced by neurotransmitters. Nature. 1994, 368: 140-144. 10.1038/368140a0.CrossRefPubMed
36.
37.
Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G: Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. The EMBO journal. 2009, 28: 697-710. 10.1038/emboj.2009.10.PubMedCentralCrossRefPubMed
38.
Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, Bassell GJ, Condeelis J, Singer RH: Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature. 2005, 438: 512-515. 10.1038/nature04115.CrossRefPubMed
39.
Metadata
Title
Regulation of chemotropic guidance of nerve growth cones by microRNA
Authors
Liang Han
Zhexing Wen
Rachel C Lynn
Marie-Laure Baudet
Christine E Holt
Yukio Sasaki
Gary J Bassell
James Q Zheng
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Molecular Brain / Issue 1/2011
Electronic ISSN: 1756-6606
DOI
https://doi.org/10.1186/1756-6606-4-40

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