MiR-21 is an Ngf-modulated MicroRNA That supports Ngf signaling and regulates neuronal degeneration in PC12 cells

NeuroMolecular Medicine

Volumn 16, Issue 2, 2014, Pages 415-430

  Montalban, Enrica ^a,b,e   Mattugini, Nicola ^a,c,f   Ciarapica, Roberta ^b   Provenzano, Claudia ^c   Savino, Mauro ^a   Scagnoli, Fiorella ^a,c   Prosperini, Gianluca ^d   Carissimi, Claudia ^a   Fulci, Valerio ^a   Matrone, Carmela ^c,g   Calissano, Pietro ^b   Nasi, Sergio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^c CNR   (Italy)

^d CINECA   (Italy)

^e INSTITUT DU FER À MOULIN   (France)

^f UNIVERSITY OF MUNICH   (Germany)

^g AARHUS UNIVERSITY   (Denmark)

Author keywords

Differentiation; Gene expression; MicroRNA; Neurodegeneration; Neurotrophins; Signaling

Indexed keywords

MICRORNA; MICRORNA 103; MICRORNA 132; MICRORNA 207; MICRORNA 21; MICRORNA 29C; MICRORNA 30C; MICRORNA 691; MICRORNA 709; MICRORNA 93; NERVE GROWTH FACTOR; UNCLASSIFIED DRUG; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MIRN21 MICRORNA, RAT; RNA;

ARTICLE; CELL PROTECTION; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; NERVE CELL NETWORK; NERVE DEGENERATION; NEURITE; PC12 CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; DEGENERATIVE DISEASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PHYSIOLOGY; RAT; ULTRASTRUCTURE;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; MICRORNAS; NERVE GROWTH FACTOR; NEURITES; NEURODEGENERATIVE DISEASES; NEUROGENESIS; NEURONS; PC12 CELLS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, NEOPLASM; SIGNAL TRANSDUCTION;

EID: 84901339622     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-014-8292-z     Document Type: Article

References (53)

1. Adilakshmi, T., Sudol, I., & Tapinos, N. (2012). Combinatorial action of miRNAs regulates transcriptional and post-transcriptional gene silencing following in vivo PNS injury. PLoS ONE, 7(7), e39674.
2. Alsina, F. C., Irala, D., Fontanet, P. A., Hita, F. J., Ledda, F., & Paratcha, G. (2012). Sprouty4 is an endogenous negative modulator of TrkA signaling and neuronal differentiation induced by Ngf. PLoS ONE, 7(2), e32087.
3. Annibali, D., Gioia, U., Savino, M., Laneve, P., Caffarelli, E., & Nasi, S. (2012). A new module in neural differentiation control: Two microRNA upregulated by Retinoic Acid, miR-9 and-103, target the differentiation inhibitor ID2. PLoS ONE, 7(7), e40269.
4. Annibali, D., & Nasi, S. (2007). Signaling by neurotrophins. In Reactome. http://www.reactome.org.
5. Babenko, O., Golubov, A., Ilnytskyy, Y., Kovalchuk, I., & Metz, G. A. (2012). Genomic and epigenomic responses to chronic stress involve miRNA-mediated programming. PLoS ONE, 7(1), e29441.
6. Bhalala, O. G., Pan, L., Sahni, V., McGuire, T. L., Gruner, K., Tourtellotte, W. G., et al. (2012). MicroRNA-21 regulates astrocytic response following spinal cord injury. The Journal of Neuroscience, 32(50), 17935-17947.
7. Brett, J. O., Renault, V. M., Rafalski, V. A., Webb, A. E., & Brunet, A. (2008). The microRNA cluster miR-106b-25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging (Albany NY), 3(2), 108-124.
8. Buller, B., Liu, X., Wang, X., Zhang, R. L., Zhang, L., Hozeska-Solgot, A., et al. (2010). miR-21 protects neurons from ischemic death. FEBS Journal, 277(20), 4299-4307.
9. Calissano, P., Matrone, C., & Amadoro, G. (2010). Nerve growth factor as a paradigm of neurotrophins related to Alzheimer's disease. Developmental Neurobiology, 70(5), 372-383.
10. Chao, M. V., Rajagopal, R., & Lee, F. S. (2006). Neurotrophin signaling in health and disease. Clinical Science, 110(2), 167-173.
11. DIANA LAB - DNA Intelligent Analysis. (2013). http://diana.cslab.ece. ntua.gr.
12. Ebert, M. S., Neilson, J. R., & Sharp, P. A. (2007). MicroRNA sponges: Competitive inhibitors of small RNAs in mammalian cells. Nature Methods, 4(9), 721-726.
13. Gentner, B., Schira, G., Giustacchini, A., Amendola, M., Brown, B. D., Ponzoni, M., et al. (2009). Stable knockdown of microRNA in vivo by lentiviral vectors. Nature Methods, 6(1), 63-66.
14. Greene, L. A. (1978). Nerve growth factor prevents the death and stimulates the neural differentiation of clonal PC12 pheochromocytoma cells in serum-free medium. The Journal of Cell Biology, 78(3), 747-755.
15. Greene, L. A., & Tischler, A. S. (1976). Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proceedings of the National Academy of Sciences of the United States of America, 73(7), 2424-2428.
16. Hatley, M. E., Patrick, D. M., Garcia, M. R., Richardson, J. A., Bassel-Duby, R., van Rooij, E., et al. (2010). Modulation of K-Ras-dependent lung tumorigenesis by microRNA-21. Cancer Cell, 18(3), 282-293.
17. Hausott, B., Vallant, N., Auer, M., Yang, L., Dai, F., Brand-Saberi, B., et al. (2009). Sprouty2 down-regulation promotes axon growth by adult sensory neurons. Molecular and Cellular Neuroscience, 42(4), 328-340.
18. Im, H. I., Hollander, J. A., Bali, P., Kenny, P. J., et al. (2010). MeCP2 controls Bdnf expression and cocaine intake through homeostatic interactions with microRNA-212. Nature Neuroscience, 13(9), 1120-1127.
19. Impey, S., Davare, M., Lesiak, A., Fortin, D., Ando, H., Varlamova, O., et al. (2010). An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Molecular and Cellular Neuroscience, 43(1), 146-156.
20. Kaplan, D. R., & Miller, F. D. (2000). Neurotrophin signal transduction in the nervous system. Current Opinion in Neurobiology, 10(3), 381-391.
21. KEGG PATHWAY database. (2013). http://www.genome.jp/kegg/pathway.html.
22. Kosik, K. S. (2006). The neuronal microRNA system. Nature Reviews Neuroscience, 7(12), 911-920.
23. Krichevsky, A. M., & Gabriely, G. (2009). miR-21 a small multi-faceted RNA. Journal of Cellular and Molecular Medicine, 13(1), 39-53.
24. Lee, S. T., Chu, K., Im, W. S., Yoon, H. J., Im, J. Y., Park, J. E., et al. (2011). Altered microRNA regulation in Huntington's disease models. Experimental Neurology, 227(1), 172-179.
25. Levi, A., Ferri, G. L., Watson, E., Possenti, R., & Salton, S. R. (2004). Processing, distribution, and function of VGF, a neuronal and endocrine peptide precursor. Cellular and Molecular Neurobiology, 24(4), 517-533.
26. Loscher, C. J., Hokamp, K., Kenna, P. F., Ivens, A. C., Humphries, P., Palfi, A., et al. (2008). Altered retinal microRNA expression profile in a mouse model of retinitis pigmentosa. Genome Biology, 8(11), R248.
27. Luikart, B. W., Bensen, A. L., Washburn, E. K., Perederiy, J. V., Su, K. G., Li, Y., et al. (2011). miR-132 mediates the integration of newborn neurons into the adult dentate gyrus. PLoS ONE, 6(5), e19077.
28. Maes, O. C., Chertkow, H. M., Wang, E., & Schipper, H. M. (2009). MicroRNA: Implications for Alzheimer disease and other human CNS disorders. Current Genomics, 10(3), 154-168.
29. Mandolesi, G., Gargano, S., Pennuto, M., Illi, B., Molfetta, R., Soucek, L., et al. (2002). Ngf-dependent and tissue-specific transcription of Vgf is regulated by a Creb-p300 and bHLH factor interaction. FEBS Letter, 510(1-2), 50-56.
30. Marson, A., Levine, S. S., Cole, M. F., Frampton, G. M., Brambrink, T., Johnstone, S., et al. (2008). Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell, 134(3), 521-533.
31. Matrone, C., Ciotti, M. T., Mercanti, D., Marolda, R., & Calissano, P. (2008a). Ngf and Bdnf signaling control amyloidogenic route and Aβ production in hippocampal neurons. Proceedings of the National Academy of Sciences of the United States of America, 105(35), 13139-13144. Epub 2008 Aug 26.
32. Matrone, C., Di Luzio, A., Meli, G., D'Aguanno, S., Severini, C., Ciotti, M. T., et al. (2008b). Activation of the amyloidogenic route by Ngf deprivation induces apoptotic death in PC12 cells. Journal of Alzheimers Disease, 13(1), 81-96.
33. Mei, Y., Bian, C., Li, J., Du, Z., Zhou, H., Yang, Z., et al. (2012). miR-21 modulates the Erk-MapK signaling pathway by regulating Spry2 expression during human mesenchymal stem cell differentiation. Journal of Cellular Biochemistry, 114(6), 1374-1384.
34. Mellios, N., Huang, H. S., Grigorenko, A., Rogaev, E., & Akbarian, S. (2008). A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of Bdnf in prefrontal cortex. Human Molecular Genetics, 17(19), 3030-3042.
35. Mesner, P. W., Epting, C. L., Hegarty, J. L., & Green, S. H. (1995). A timetable of events during programmed cell death induced by trophic factor withdrawal from neuronal PC12 cells. The Journal of Neuroscience, 15(11), 7357-7366.
36. Miller, B. H., & Wahlestedt, C. (2012). MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proceedings of the National Academy of Sciences of the United States of America, 109(8), 3125-3130.
37. Mullenbrock, S., Shah, J., & Cooper, G. M. (2012). Global expression analysis identified a preferentially nerve growth factor-induced transcriptional program regulated by sustained mitogen-activated protein kinase/extracellular signal-regulated kinase (Erk) and AP-1 protein activation during PC12 cell differentiation. The Journal of biological chemistry, 286(52), 45131-45145.
38. Papagiannakopoulos, T., Shapiro, A., & Kosik, K. S. (2008). MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Research, 68, 8164-8172.
39. Paschou, M., Paraskevopoulou, M. D., Vlachos, I. S., Koukouraki, P., Hatzigeorgiou, A. G., & Doxakis, E. (2012). miRNA regulons associated with synaptic function. PLoS ONE, 7(10), e46189.
40. Remenyi, J., Hunter, C. J., Cole, C., Ando, H., Impey, S., Monk, C. E., et al. (2010). Regulation of the miR-212/132 locus by MSK1 and Creb in response to neurotrophins. Biochemical Journal, 428(2), 281-289.
41. Strickland, I. T., Richards, L., Holmes, F. E., Wynick, D., Uney, J. B., & Wong, L. F. (2011). Axotomy-Induced miR-21 promotes axon growth in adult dorsal root ganglion neurons. PLoS ONE, 6(8), e23423.
42. Talotta, F., Cimmino, A., Matarazzo, M. R., Casalino, L., De Vita, G., D'Esposito, M., et al. (2009). An autoregulatory loop mediated by miR-21 and PDCD4 controls the AP-1 activity in RAS transformation. Oncogene, 28(1), 73-84.
43. Terasawa, K., Ichimura, A., Sato, F., Shimizu, K., & Tsujimoto, G. (2006). Sustained activation of Erk1/2 by Ngf induces microRNA-221 and 222 in PC12 cells. FEBS Journal, 276(12), 3269-3276.
44. The Gene Expression Omnibus. (2013). http://www.ncbi.nlm.nih.gov/geo.
45. The JASPAR database. (2013). http://jaspar.genereg.net.
46. Tognini, P., Putignano, E., Coatti, A., & Pizzorusso, T. (2011). Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nature Neuroscience, 14(10), 1237-1239.
47. Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., et al. (2005). cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16426-16431.
48. Wanet, A., Tacheny, A., Arnould, T., & Renard, P. (2012). miR-212/132 expression and functions: Within and beyond the neuronal compartment. Nucleic Acids Research, 40(11), 4742-4753.
49. Wang, P., Zou, F., Zhang, X., Li, H., Dulak, A., Tomko, R. J., Jr, et al. (2009). MicroRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Research, 69, 8157-8165.
50. Yao, J., Hennessey, T., Flynt, A., Lai, E., Beal, M. F., & Lin, M. T. (2010). MicroRNA-related cofilin abnormality in Alzheimer's disease. PLoS ONE, 5(12), e15546.
51. Zhang, Y. W., Thompson, R., Zhang, H., & Xu, H. (2011). App processing in Alzheimer's disease. Molecular Brain, 4, 3.
52. Zhang, L., Dong, L. Y., Li, Y. J., Hong, Z., & Wei, W. S. (2012). miR-21 represses FasL in microglia and protects against microglia-mediated neuronal cell death following hypoxia/ischemia. Glia, 60(12), 1888-1895.
53. Zong, Y., Wang, H., Dong, W., Quan, X., Zhu, H., Xu, Y., et al. (2011). miR-29c regulates Bace1 protein expression. Brain Research, 1395, 108-115.