Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology

Journal of Cell Biology

Volumn 194, Issue 6, 2011, Pages 889-904

  Lippi, Giordano ^a,e   Steinert, Joern R ^a   Marczylo, Emma L ^a   D'Oro, Sabina ^c   Fiore, Roberto ^b,f   Forsythe, Ian D ^a   Schratt, Gerhard ^b,f   Zoli, Michele ^c   Nicotera, Pierluigi ^d   Young, Kenneth W ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e NEUROBIOLOGY SECTION   (United States)

^f PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; AMPHETAMINE; COCAINE; CYTOSKELETON PROTEIN; MICRORNA; MICRORNA 29A; MICRORNA 29B; NICOTINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CYTOSKELETON; DENDRITIC SPINE; DOWN REGULATION; HIPPOCAMPUS; HUMAN; IN VITRO STUDY; MORPHOLOGICAL ADAPTATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE;

BASIDIOMYCOTA; MUS;

EID: 80053938493     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201103006     Document Type: Article

References (66)

1. Bacci, A., C. Verderio, E. Pravettoni, and M. Matteoli. 1999. Synaptic and intrinsic mechanisms shape synchronous oscillations in hippocampal neurons in culture. Eur. J. Neurosci. 11:389-397.
2. Bartel, D.P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 116:281-297.
3. Bartel, D.P. 2009. MicroRNAs: target recognition and regulatory functions. Cell. 136:215-233.
4. Chandrasekar, V., and J.L. Dreyer. 2009. microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol. Cell. Neurosci. 42:350-362.
5. Christensen, M., and G.M. Schratt. 2009. microRNA involvement in developmental and functional aspects of the nervous system and in neurological diseases. Neurosci. Lett. 466:55-62.
6. Dillon, C., and Y. Goda. 2005. The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28:25-55.
7. Dunaevsky, A., A. Tashiro, A. Majewska, C. Mason, and R. Yuste. 1999. Developmental regulation of spine motility in the mammalian central nervous system. Proc. Natl. Acad. Sci. USA. 96:13438-13443.
8. Edbauer, D., J.R. Neilson, K.A. Foster, C.F. Wang, D.P. Seeburg, M.N. Batterton, T. Tada, B.M. Dolan, P.A. Sharp, and M. Sheng. 2010. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron. 65:373-384.
9. Engert, F., and T. Bonhoeffer. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature. 399:66-70.
10. Fineberg, S.K., K.S. Kosik, and B.L. Davidson. 2009. MicroRNAs potentiate neural development. Neuron. 64:303-309.
11. Fiore, R., S. Khudayberdiev, M. Christensen, G. Siegel, S.W. Flavell, T.K. Kim, M.E. Greenberg, and G. Schratt. 2009. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 28:697-710.
12. Fischer, M., S. Kaech, U. Wagner, H. Brinkhaus, and A. Matus. 2000. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat. Neurosci. 3:887-894.
13. Fischer, A., F. Sananbenesi, C. Schrick, J. Spiess, and J. Radulovic. 2004. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear. J. Neurosci. 24:1962-1966.
14. Gao, J., W.Y. Wang, Y.W. Mao, J. Gräff, J.S. Guan, L. Pan, G. Mak, D. Kim, S.C. Su, and L.H. Tsai. 2010. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature. 466:1105-1109.
15. Goley, E.D., and M.D. Welch. 2006. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7:713-726.
16. Gournier, H., E.D. Goley, H. Niederstrasser, T. Trinh, and M.D. Welch. 2001. Reconstitution of human Arp2/3 complex reveals critical roles of individual subunits in complex structure and activity. Mol. Cell. 8:1041-1052.
17. Grabrucker, A., B. Vaida, J. Bockmann, and T.M. Boeckers. 2009. Synaptogenesis of hippocampal neurons in primary cell culture. Cell Tissue Res. 338:333-341.
18. Greer, P.L., and M.E. Greenberg. 2008. From synapse to nucleus: calciumdependent gene transcription in the control of synapse development and function. Neuron. 59:846-860.
19. Guo, H., N.T. Ingolia, J.S. Weissman, and D.P. Bartel. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 466:835-840.
20. Hébert, S.S., K. Horré, L. Nicolaï, A.S. Papadopoulou, W. Mandemakers, A.N. Silahtaroglu, S. Kauppinen, A. Delacourte, and B. De Strooper. 2008. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc. Natl. Acad. Sci. USA. 105:6415-6420.
21. Hollander, J.A., H.I. Im, A.L. Amelio, J. Kocerha, P. Bali, Q. Lu, D. Willoughby, C. Wahlestedt, M.D. Conkright, and P.J. Kenny. 2010. Striatal microRNA controls cocaine intake through CREB signalling. Nature. 466:197-202.
22. Hotulainen, P., O. Llano, S. Smirnov, K. Tanhuanpää, J. Faix, C. Rivera, and P. Lappalainen. 2009. Defining mechanisms of actin polymerization anddepolymerization during dendritic spine morphogenesis. J. Cell Biol. 185:323-339.
23. Im, H.I., J.A. Hollander, P. Bali, and P.J. Kenny. 2010. MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat. Neurosci. 13:1120-1127.
24. Impey, S., M. Davare, A. Lasiek, D. Fortin, H. Ando, O. Varlamova, K. Obrietan, T.R. Soderling, R.H. Goodman, and G.A. Wayman. 2010. An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol. Cell. Neurosci. 43:146-156.
25. Kim, V.N., J.J. Han, and M.C. Siomi. 2009. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10:126-139.
26. Knafo, S., G. Ariav, E. Barkai, and F. Libersat. 2004. Olfactory learning-induced increase in spine density along the apical dendrites of CA1 hippocampal neurons. Hippocampus. 14:819-825.
27. Korkotian, E., and M. Segal. 2001. Regulation of dendritic spine motility in cultured hippocampal neurons. J. Neurosci. 21:6115-6124.
28. Kosik, K.S. 2006. The neuronal microRNA system. Nat. Rev. Neurosci. 7:911-920.
29. Krol, J., V. Busskamp, I. Markiewicz, M.B. Stadler, S. Ribi, J. Richter, J. Duebel, S. Bicker, H.J. Fehling, D. Schübeler, et al. 2010. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell. 141:618-631.
30. Lamprecht, R., and J. LeDoux. 2004. Structural plasticity and memory. Nat. Rev. Neurosci. 5:45-54.
31. Lee, R.C., R.L. Feinbaum, and V. Ambros. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:843-854.
32. Lee, Y., K. Jeon, J.T. Lee, S. Kim, and V.N. Kim. 2002. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21:4663-4670.
33. Leuner, B., J. Falduto, and T.J. Shors. 2003. Associative memory formation increases the observation of dendritic spines in the hippocampus. J. Neurosci. 23:659-665.
34. Lewis, B.P., C.B. Burge, and D.P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell. 120:15-20.
35. Lim, L.P., N.C. Lau, P. Garrett-Engele, A. Grimson, J.M. Schelter, J. Castle, D.P. Bartel, P.S. Linsley, and J.M. Johnson. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 433:769-773.
36. -ΔΔCT Method. Methods. 25:402-408.
37. Lugli, G., J. Larson, M.E. Martone, Y. Jones, and N.R. Smalheiser. 2005. 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. 94:896-905.
38. McClung, C.A., and E.J. Nestler. 2003. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci. 6:1208-1215.
39. McClung, C.A., and E.J. Nestler. 2008. Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology. 33:3-17.
40. Miska, E.A., E. Alvarez-Saavedra, M. Townsend, A. Yoshii, N. Sestan, P. Rakic, M. Constantine-Paton, and H.R. Horvitz. 2004. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 5:R68.
41. Ogura, A., T. Iijima, T. Amano, and Y. Kudo. 1987. Optical monitoring of excitatory synaptic activity between cultured hippocampal neurons by a multi-site Ca2+ fluorometry. Neurosci. Lett. 78:69-74.
42. Papa, M., and M. Segal. 1996. Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience. 71:1005-1011.
43. Rajasethupathy, P., F. Fiumara, R. Sheridan, D. Betel, S.V. Puthanveettil, J.J. Russo, C. Sander, T. Tuschl, and E. Kandel. 2009. Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron. 63:803-817.
44. Restivo, L., G. Vetere, B. Bontempi, and M. Ammassari-Teule. 2009. The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J. Neurosci. 29:8206-8214.
45. Richards, D.A., J.M. Mateos, S. Hugel, V. de Paola, P. Caroni, B.H. Gähwiler, and R.A. McKinney. 2005. Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures. Proc. Natl. Acad. Sci. USA. 102:6166-6171.
46. Robinson, T.E., and B. Kolb. 2004. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology. 47(Suppl 1):33-46.
47. Russo, S.J., C.A. Bolanos, D.E. Theobald, N.A. DeCarolis, W. Renthal, A. Kumar, C.A. Winstanley, N.E. Renthal, M.D. Wiley, D.W. Self, et al. 2007. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat. Neurosci. 10:93-99.
48. Russo, S.J., D.M. Dietz, D. Dumitriu, J.H. Morrison, R.C. Malenka, and E.J. Nestler. 2010. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33:267-276.
49. Saneyoshi, T., D.A. Fortin, and T.R. Soderling. 2010. Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr. Opin. Neurobiol. 20:108-115.
50. Schratt, G. 2009. microRNAs at the synapse. Nat. Rev. Neurosci. 10:842-849.
51. Schratt, G.M., F. Tuebing, E.A. Nigh, C.G. Kane, M.E. Sabatini, M. Kiebler, and M.E. Greenberg. 2006. A brain-specific microRNA regulates dendritic spine development. Nature. 439:283-289.
52. Sempere, L.F., S. Freemantle, I. Pitha-Rowe, E. Moss, E. Dmitrovsky, and V. Ambros. 2004. 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.
53. Siegel, G., G. Obernosterer, R. Fiore, M. Oehmen, S. Bicker, M. Christensen, S. Khudayberdiev, P.F. Leuschner, C.J.L. Busch, C. Kane, et al. 2009. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 11:705-716.
54. Star, E.N., D.J. Kwiatkowski, and V.N. Murthy. 2002. Rapid turnover of actin in dendritic spines and its regulation by activity. Nat. Neurosci. 5:239-246.
55. Tang, J., and J.A. Dani. 2009. Dopamine enables in vivo synaptic plasticity associated with the addictive drug nicotine. Neuron. 63:673-682.
56. Toda, S., H.W. Shen, J. Peters, S. Cagle, and P.W. Kalivas. 2006. Cocaine increases actin cycling: effects in the reinstatement model of drug seeking. J. Neurosci. 26:1579-1587.
57. Vo, N., M.E. Klein, O. Varlamova, D.M. Keller, T. Yamamoto, R.H. Goodman, and S. Impey. 2005. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. USA. 102:16426-16431.
58. Walters, C.L., J.N. Cleck, Y.-C. Kuo, and J.A. Blendy. 2005. μ-Opioid receptor and CREB activation are required for nicotine reward. Neuron. 46:933-943.
59. Wayman, G.A., M. Davare, H. Ando, D. Fortin, O. Varlamova, H.Y. Cheng, D. Marks, K. Obrietan, T.R. Soderling, R.H. Goodman, and S. Impey. 2008. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl. Acad. Sci. USA. 105:9093-9098.
60. West, A.E., E.C. Griffith, and M.E. Greenberg. 2002. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3:921-931.
61. Wightman, B., I. Ha, and G. Ruvkun. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 75:855-862.
62. Winter, J., S. Jung, S. Keller, R.I. Gregory, and S. Diederichs. 2009. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 11:228-234.
63. Yang, G., F. Pan, and W.-B. Gan. 2009. Stably maintained dendritic spines are associated with lifelong memories. Nature. 462:920-924.
64. 2+ signalling in hippocampal neurons. Cell Calcium. 43:296-306.
65. Zanardi, A., R. Ferrari, G. Leo, U. Maskos, J.P. Changeux, and M. Zoli. 2007. Loss of high-affinity nicotinic receptors increases the vulnerability to excitotoxic lesion and decreases the positive effects of an enriched environment. FASEB J. 21:4028-4037.
66. Ziviani, E., G. Lippi, D. Bano, E. Munarriz, S. Guiducci, M. Zoli, K.W. Young, and P. Nicotera. 2011. Ryanodine receptor-2 upregulation and nicotinemediated plasticity. EMBO J. 30:194-204.