MicroRNAs in neurons: Manifold regulatory roles at the synapse

Current Opinion in Genetics and Development

Volumn 21, Issue 4, 2011, Pages 491-497

  Siegel, Gabriele ^a   Saba, Reuben ^a   Schratt, Gerhard ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MICRORNA; SYNAPSE RECEPTOR;

ELECTROENCEPHALOGRAM; GENE TARGETING; GENETIC REGULATION; HUMAN; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

3' UNTRANSLATED REGIONS; ANIMALS; BRAIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICRORNAS; RNA, SMALL UNTRANSLATED; SYNAPSES;

EID: 79960903902     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2011.04.008     Document Type: Review

References (43)

1. Huntzinger E., Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011, 12:99-110.
2. Giraldez A.J., Cinalli R.M., Glasner M.E., Enright A.J., Thomson J.M., Baskerville S., Hammond S.M., Bartel D.P., Schier A.F. MicroRNAs regulate brain morphogenesis in zebrafish. Science (New York, NY) 2005, 308:833-838.
3. Kim J., Inoue K., Ishii J., Vanti W.B., Voronov S.V., Murchison E., Hannon G., Abeliovich A. A microRNA feedback circuit in midbrain dopamine neurons. Science (New York, NY) 2007, 317:1220-1224.
4. Schaefer A., O'Carroll D., Tan C.L., Hillman D., Sugimori M., Llinas R., Greengard P. Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med 2007, 204:1553-1558.
5. Cuellar T.L., Davis T.H., Nelson P.T., Loeb G.B., Harfe B.D., Ullian E., McManus M.T. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci USA 2008, 105:5614-5619.
6. De Pietri Tonelli D., Pulvers J.N., Haffner C., Murchison E.P., Hannon G.J., Huttner W.B. miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development (Cambridge, England) 2008, 135:3911-3921.
7. Davis T.H., Cuellar T.L., Koch S.M., Barker A.J., Harfe B.D., McManus M.T., Ullian E.M. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci: Offic J Soc Neurosci 2008, 28:4322-4330.
8. Kawase-Koga Y., Low R., Otaegi G., Pollock A., Deng H., Eisenhaber F., Maurer-Stroh S., Sun T. RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cells. J Cell Sci 2010, 123:586-594.
9. Konopka W., Kiryk A., Novak M., Herwerth M., Parkitna J.R., Wawrzyniak M., Kowarsch A, Michaluk P, Dzwonek J., Arnsperger T., et al. MicroRNA loss enhances learning and memory in mice. J Neurosci: Offic J Soc Neurosci 2010, 30:14835-14842.
10. Richter J.D., Klann E. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Devel 2009, 23:1-11.
11. Kye M.J., Liu T., Levy S.F., Xu N.L., Groves B.B., Bonneau R., Lao K., Kosik K.S. Somatodendritic microRNAs identified by laser capture and multiplex RT-PCR. RNA (New York, NY) 2007, 13:1224-1234.
12. Lugli G., Torvik V.I., Larson J., Smalheiser N.R. Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. J Neurochem 2008, 106:650-661.
13. Siegel G., Obernosterer G., Fiore R., Oehmen M., Bicker S., Christensen M., Khudayberdiev S., Leuschner P.F., Busch C.J., Kane C., et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat Cell Biol 2009, 11:705-716.
14. Natera-Naranjo O., Aschrafi A., Gioio A.E., Kaplan B.B. Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons. RNA (New York, NY) 2010, 16:1516-1529.
15. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., Greenberg M.E. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
16. Bernard O. Lim kinases, regulators of actin dynamics. Int J Biochem Cell Biol 2007, 39:1071-1076.
17. Gao J., Wang W.Y., Mao Y.W., Graff J., Guan J.S., Pan L., Mak G., Kim D., Su S.C., Tsai L.H. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 2010, 466:1105-1109.
18. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 2009, 89:121-145.
19. Bhattacharyya R., Wedegaertner P.B. Galpha 13 requires palmitoylation for plasma membrane localization, Rho-dependent signaling, and promotion of p115-RhoGEF membrane binding. J Biol Chem 2000, 275:14992-14999.
20. Vo N., Klein M.E., Varlamova O., Keller D.M., Yamamoto T., Goodman R.H., Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci USA 2005, 102:16426-16431.
21. Wayman G.A., Davare M., Ando H., Fortin D., Varlamova O., Cheng H.Y., Marks D., Obrietan K., Soderling T.R., Goodman R.H., et al. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc Natl Acad Sci USA 2008, 105:9093-9098.
22. Magill S.T., Cambronne X.A., Luikart B.W., Lioy D.T., Leighton B.H., Westbrook G.L., Mandel G., Goodman R.H. microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci USA 2010, 107:20382-20387.
23. Hansen K.F., Sakamoto K., Wayman G.A., Impey S., Obrietan K. Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One 2010, 5:e15497.
24. Impey S., Davare M., Lasiek A., Fortin D., Ando H., Varlamova O., Obrietan K., Soderling T.R., Goodman R.H., Wayman G.A. An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol Cell Neurosci 2010, 43:146-156.
25. Edbauer D., Neilson J.R., Foster K.A., Wang C.F., Seeburg D.P., Batterton M.N., Tada T., Dolan B.M., Sharp P.A., Sheng M. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 2010, 65:373-384.
26. Bagni C., Greenough W.T. From mRNP trafficking to spine dysmorphogenesis: the roots of fragile X syndrome. Nat Rev-Neurosci 2005, 6:376-387.
27. Rajasethupathy P., Fiumara F., Sheridan R., Betel D., Puthanveettil S.V., Russo J.J., Sander C., Tuschl T., Kandel E. Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 2009, 63:803-817.
28. Fiore R., Khudayberdiev S., Christensen M., Siegel G., Flavell S.W., Kim T.K., Greenberg M.E., Schratt G. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 2009, 28:697-710.
29. Krol J., Busskamp V., Markiewicz I., Stadler M.B., Ribi S., Richter J., Duebel J., Bicker S., Fehling H.J., Schubeler D., et al. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 2010, 141:618-631.
30. Lugli G., Larson J., Martone M.E., Jones Y., Smalheiser N.R. Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner. J Neurochem 2005, 94:896-905.
31. Ashraf S.I., McLoon A.L., Sclarsic S.M., Kunes S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 2006, 124:191-205.
32. Banerjee S., Neveu P., Kosik K.S. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 2009, 64:871-884.
33. Li Y., Lin L., Jin P. The microRNA pathway and fragile X mental retardation protein. Biochim Biophys Acta 2008, 1779:702-705.
34. Muddashetty R.S., Kelic S., Gross C., Xu M., Bassell G.J. Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J Neurosci: Offic J Soc Neurosci 2007, 27:5338-5348.
35. Narayanan U., Nalavadi V., Nakamoto M., Pallas D.C., Ceman S., Bassell G.J., Warren S.T. FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 2007, 27:14349-14357.
36. Vasudevan S., Tong Y., Steitz J.A. Switching from repression to activation: microRNAs can up-regulate translation. Science 2007, 318:1931-1934.
37. Stark K.L., Xu B., Bagchi A., Lai W.S., Liu H., Hsu R., Wan X., Pavlidis P., Mills A.A., Karayiorgou M., et al. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat Genet 2008, 40:751-760.
38. Fenelon K., Mukai J., Xu B., Hsu P.K., Drew L.J., Karayiorgou M., Fischbach G.D., Macdermott A.B., Gogos J.A. Deficiency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proc Natl Acad Sci USA 2011, 108:4447-4452.
39. Jin P., Zarnescu D.C., Ceman S., Nakamoto M., Mowrey J., Jongens T.A., Nelson D.L., Moses K., Warren S.T. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 2004, 7:113-117.
40. Didiot M.C., Subramanian M., Flatter E., Mandel J.L., Moine H. Cells lacking the fragile X mental retardation protein (FMRP) have normal RISC activity but exhibit altered stress granule assembly. Mol Biol Cell 2009, 20:428-437.
41. Xu X.L., Li Y., Wang F., Gao F.B. The steady-state level of the nervous-system-specific microRNA-124a is regulated by dFMR1 in Drosophila. J Neurosci: Offic J Soc Neurosci 2008, 28:11883-11889.
42. Klein M.E., Lioy D.T., Ma L., Impey S., Mandel G., Goodman R.H. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci 2007, 10:1513-1514.
43. Kocerha J., Faghihi M.A., Lopez-Toledano M.A., Huang J., Ramsey A.J., Caron M.G., Sales N., Willoughby D., Elmen J., Hansen H.F., et al. MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc Natl Acad Sci USA 2009, 106:3507-3512.