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MiR-34 and MiR-200: Regulator of Cell Fate Plasticity and Neural Development

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Abstract

Studies from last two decades have established microRNAs (miRNAs) as the most influential regulator of gene expression, especially at the post-transcriptional stage. The family of small RNA molecules including miRNAs is highly conserved and expressed throughout the multicellular organism. MiRNAs regulate gene expression by binding to 3′ UTR of protein-coding mRNAs and initiating either decay or movement of mRNAs to stress granules. Tissues or cells, which go through cell fate transformation like stem cells, brain cells, iPSCs, or cancer cells show very dynamic expression profile of miRNAs. Inability to pass the developmental stages of Dicer (miRNA maturation enzyme) knockout animals has confirmed that expression of mature and functional miRNAs is essential for proper development of different organs and tissues. Studies from our laboratory and elsewhere have demonstrated the role of miR-200 and miR-34 families in neural development and have shown higher expression of both families in mature and differentiated neurons. In present review, we have provided a general overview of miRNAs and focused on the role of miR-34 and miR-200, two miRNA families, which have the capability to change the phenotype and fate of a cell in different tissues and situations.

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References

  • Aberdam, D., Candi, E., Knight, R. A., & Melino, G. (2008). miRNAs, ‘stemness’ and skin. Trends in Biochemical Sciences, 33(12), 583–591.

    Article  CAS  PubMed  Google Scholar 

  • Agostini, M., Tucci, P., Killick, R., Candi, E., Sayan, B. S., di val Cervo, P. R., et al. (2011). Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proceedings of the National Academy of Sciences, 108(52), 21093–21098.

    Article  Google Scholar 

  • Alvarez-Garcia, I., & Miska, E. A. (2005). MicroRNA functions in animal development and human disease. Development, 132(21), 4653–4662.

    Article  CAS  PubMed  Google Scholar 

  • Amaral, P. P., & Mattick, J. S. (2008). Noncoding RNA in development. Mammalian Genome, 19(7–8), 454–492.

    Article  CAS  PubMed  Google Scholar 

  • Ambros, V., Bartel, B., Bartel, D. P., Burge, C. B., Carrington, J. C., Chen, X., et al. (2003). A uniform system for microRNA annotation. RNA, 9(3), 277–279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen, S. L. (2003). Trajectories of brain development: point of vulnerability or window of opportunity? Neuroscience and Biobehavioral Reviews, 27(1), 3–18.

    Article  PubMed  Google Scholar 

  • Aranha, M. M., Santos, D. M., Solá, S., Steer, C. J., & Rodrigues, C. (2011). miR-34a regulates mouse neural stem cell differentiation. PLoS ONE, 6(8), e21396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell, M. J., & Bartel, D. P. (2005). Antiquity of microRNAs and their targets in land plants. The Plant Cell, 17(6), 1658–1673.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azari, H., & Reynolds, B. A. (2016). In vitro models for neurogenesis. Cold Spring Harbor Perspectives in Biology, 8(6), a021279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartel, D. P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116(2), 281–297.

    Article  CAS  PubMed  Google Scholar 

  • Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., et al. (2003). Dicer is essential for mouse development. Nature Genetics, 35(3), 215–217.

    Article  CAS  PubMed  Google Scholar 

  • Bhaskaran, M., & Mohan, M. (2014). MicroRNAs: History, biogenesis, and their evolving role in animal development and disease. Veterinary Pathology, 51(4), 759–774.

    Article  CAS  PubMed  Google Scholar 

  • Brabletz, S., & Brabletz, T. (2010). The ZEB/miR-200 feedback loop—A motor of cellular plasticity in development and cancer? EMBO Reports, 11(9), 670–677.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B., & Cohen, S. M. (2003). Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell, 113(1), 25–36.

    Article  CAS  PubMed  Google Scholar 

  • Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., et al. (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Reports, 9(6), 582–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burmistrova, O., Goltsov, A., Abramova, L., Kaleda, V., Orlova, V., & Rogaev, E. (2007). MicroRNA in schizophrenia: genetic and expression analysis of miR-130b (22q11). Biochemistry (Moscow), 72(5), 578–582.

    Article  CAS  Google Scholar 

  • Cao, X., Pfaff, S. L., & Gage, F. H. (2007). A functional study of miR-124 in the developing neural tube. Genes & Development, 21(5), 531–536.

    Article  CAS  Google Scholar 

  • Carleton, M., Cleary, M. A., & Linsley, P. S. (2007). MicroRNAs and cell cycle regulation. Cell Cycle, 6(17), 2127–2132.

    Article  CAS  PubMed  Google Scholar 

  • Chen, F., & Hu, S. J. (2012). Effect of microRNA-34a in cell cycle, differentiation, and apoptosis: A review. Journal of Biochemical and Molecular Toxicology, 26(2), 79–86.

    Article  CAS  PubMed  Google Scholar 

  • Chen, K., & Rajewsky, N. (2007). The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics, 8(2), 93–103.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, L.-C., Pastrana, E., Tavazoie, M., & Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nature Neuroscience, 12(4), 399–408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, S., Zhang, C., Xu, C., Wang, L., Zou, X., & Chen, G. (2014). Age-dependent neuron loss is associated with impaired adult neurogenesis in forebrain neuron-specific Dicer conditional knockout mice. The international journal of biochemistry & cell biology, 57, 186–196.

    Article  CAS  Google Scholar 

  • Chinwalla, A. T., Cook, L. L., Delehaunty, K. D., Fewell, G. A., Fulton, L. A., Fulton, R. S., et al. (2002). Initial sequencing and comparative analysis of the mouse genome. Nature, 420(6915), 520–562.

    Article  CAS  PubMed  Google Scholar 

  • Choi, Y. J., Lin, C.-P., Ho, J. J., He, X., Okada, N., Bu, P., et al. (2011). miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nature Cell Biology, 13(11), 1353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi, Y. J., Lin, C.-P., Risso, D., Chen, S., Tan, M. H., Li, J. B., et al. (2017). Deficiency of microRNA miR-34a expands cell fate potential in pluripotent stem cells. Science, 355(6325). https://doi.org/10.1126/science.aag1927.

  • Choi, P. S., Zakhary, L., Choi, W.-Y., Caron, S., Alvarez-Saavedra, E., Miska, E. A., et al. (2008). Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron, 57(1), 41–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chua, H., Bhat-Nakshatri, P., Clare, S., Morimiya, A., Badve, S., & Nakshatri, H. (2007). NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene, 26(5), 711.

    Article  CAS  PubMed  Google Scholar 

  • Cifuentes, D., Xue, H., Taylor, D. W., Patnode, H., Mishima, Y., Cheloufi, S., et al. (2010). A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science, 328(5986), 1694–1698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colantuoni, C., Lipska, B. K., Ye, T., Hyde, T. M., Tao, R., Leek, J. T., et al. (2011). Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature, 478(7370), 519–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coolen, M., & Bally-Cuif, L. (2009). MicroRNAs in brain development and physiology. Current Opinion in Neurobiology, 19(5), 461–470.

    Article  CAS  PubMed  Google Scholar 

  • Cui, Y., Xiao, Z., Han, J., Sun, J., Ding, W., Zhao, Y., et al. (2012). MiR-125b orchestrates cell proliferation, differentiation and migration in neural stem/progenitor cells by targeting Nestin. BMC Neuroscience, 13(1), 1.

    Article  CAS  Google Scholar 

  • Datson, N. A., van der Perk, J., de Kloet, E. R., & Vreugdenhil, E. (2001). Expression profile of 30,000 genes in rat hippocampus using SAGE. Hippocampus, 11(4), 430–444.

    Article  CAS  PubMed  Google Scholar 

  • Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T., et al. (2008). Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. The Journal of Neuroscience, 28(17), 4322–4330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Antonellis, P., Medaglia, C., Cusanelli, E., Andolfo, I., Liguori, L., De Vita, G., et al. (2011). MiR-34a targeting of Notch ligand delta-like 1 impairs CD15/CD133 tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS ONE, 6(9), e24584.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du, Z.-W., Ma, L.-X., Phillips, C., & Zhang, S.-C. (2013). miR-200 and miR-96 families repress neural induction from human embryonic stem cells. Development, 140(12), 2611–2618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman, R. C., Farh, K. K.-H., Burge, C. B., & Bartel, D. P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Research, 19(1), 92–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangaraju, V. K., & Lin, H. (2009). MicroRNAs: Key regulators of stem cells. Nature Reviews Molecular Cell Biology, 10(2), 116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, F.-B. (2008). Posttranscriptional control of neuronal development by microRNA networks. Trends in Neurosciences, 31(1), 20–26.

    Article  CAS  PubMed  Google Scholar 

  • Gioia, U., Di Carlo, V., Caramanica, P., Toselli, C., Cinquino, A., Marchioni, M., et al. (2014). Mir-23a and mir-125b regulate neural stem/progenitor cell proliferation by targeting Musashi1. RNA Biology, 11(9), 1105–1112.

    Article  PubMed  PubMed Central  Google Scholar 

  • Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., Baskerville, S., et al. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science, 308(5723), 833–838.

    Article  CAS  PubMed  Google Scholar 

  • Giusti, S. A., Vogl, A. M., Brockmann, M. M., Vercelli, C. A., Rein, M. L., Trümbach, D., et al. (2014). MicroRNA-9 controls dendritic development by targeting REST. Elife, 3, e02755.

    Article  PubMed Central  Google Scholar 

  • Gonzalez, G., & Behringer, R. R. (2009). Dicer is required for female reproductive tract development and fertility in the mouse. Molecular Reproduction and Development, 76(7), 678–688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory, P. A., Bracken, C. P., Bert, A. G., & Goodall, G. J. (2008). MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle, 7(20), 3112–3117.

    Article  CAS  PubMed  Google Scholar 

  • Gregory, P. A., Bracken, C. P., Smith, E., Bert, A. G., Wright, J. A., Roslan, S., et al. (2011). An autocrine TGF-β/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Molecular Biology of the Cell, 22(10), 1686–1698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guroff, G. (1985). PC12 cells as a model of neuronal differentiation. In J. E. Bottenstein & G. Sato (Eds.), Cell culture in the neurosciences (pp. 245–272). Boston: Springer.

    Chapter  Google Scholar 

  • Gustincich, S., Sandelin, A., Plessy, C., Katayama, S., Simone, R., Lazarevic, D., et al. (2006). The complexity of the mammalian transcriptome. The Journal of Physiology, 575(2), 321–332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamada, N., Fujita, Y., Kojima, T., Kitamoto, A., Akao, Y., Nozawa, Y., et al. (2012). MicroRNA expression profiling of NGF-treated PC12 cells revealed a critical role for miR-221 in neuronal differentiation. Neurochemistry International, 60(8), 743–750.

    Article  CAS  PubMed  Google Scholar 

  • He, X., & Rosenfeld, M. G. (1991). Mechanisms of complex transcriptional regulation: implications for brain development. Neuron, 7(2), 183–196.

    Article  CAS  PubMed  Google Scholar 

  • Hermeking, H. (2010). The miR-34 family in cancer and apoptosis. Cell Death and Differentiation, 17(2), 193–199.

    Article  CAS  PubMed  Google Scholar 

  • Hohjoh, H., & Fukushima, T. (2007a). Expression profile analysis of microRNA (miRNA) in mouse central nervous system using a new miRNA detection system that examines hybridization signals at every step of washing. Gene, 391(1), 39–44.

    Article  CAS  PubMed  Google Scholar 

  • Hohjoh, H., & Fukushima, T. (2007b). Marked change in microRNA expression during neuronal differentiation of human teratocarcinoma NTera2D1 and mouse embryonal carcinoma P19 cells. Biochemical and Biophysical Research Communications, 362(2), 360–367.

    Article  CAS  PubMed  Google Scholar 

  • Hosseinahli, N., Aghapour, M., Duijf, P. H., & Baradaran, B. (2018). Treating cancer with microRNA replacement therapy: A literature review. Journal of cellular Physiology, 233, 5574–5588.

    Article  CAS  PubMed  Google Scholar 

  • Huang, T., Liu, Y., Huang, M., Zhao, X., & Cheng, L. (2010). Wnt1-cre-mediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. Journal of Molecular Cell Biology, 2(3), 152–163.

    Article  CAS  PubMed  Google Scholar 

  • Huang, B., & Zhang, R. (2014). Regulatory non-coding RNAs: revolutionizing the RNA world. Molecular Biology Reports, 41(6), 3915–3923.

    Article  CAS  PubMed  Google Scholar 

  • Humphries, B., & Yang, C. (2015). The microRNA-200 family: Small molecules with novel roles in cancer development, progression and therapy. Oncotarget, 6(9), 6472–6498.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang, H., & Mendell, J. (2006). MicroRNAs in cell proliferation, cell death, and tumorigenesis. British Journal of Cancer, 94(6), 776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivey, K. N., Muth, A., Arnold, J., King, F. W., Yeh, R.-F., Fish, J. E., et al. (2008). MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell, 2(3), 219–229.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jauhari, A., Singh, T., Pandey, A., Singh, P., Singh, N., Srivastava, A. K., et al. (2017). Differentiation induces dramatic changes in miRNA profile, where loss of dicer diverts differentiating SH-SY5Y cells toward senescence. Molecular Neurobiology, 54(7), 4986–4995.

    Article  CAS  PubMed  Google Scholar 

  • Jauhari, A., Singh, T., Singh, P., Parmar, D., & Yadav, S. (2018a). Regulation of miR-34 family in neuronal development. Molecular Neurobiology, 55(2), 936–945.

    Article  CAS  PubMed  Google Scholar 

  • Jauhari, A., Singh, T., & Yadav, S. (2018b). Expression of miR-145 and its target proteins are regulated by miR-29b in differentiated neurons. Molecular Neurobiology. https://doi.org/10.1007/s12035-018-1009-9.

    Article  PubMed  Google Scholar 

  • Jiang, F., Ye, X., Liu, X., Fincher, L., McKearin, D., & Liu, Q. (2005). Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes & Development, 19(14), 1674–1679.

    Article  CAS  Google Scholar 

  • Kalluri, R., & Weinberg, R. A. (2009). The basics of epithelial-mesenchymal transition. The Journal of Clinical Investigation, 119(6), 1420–1428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang, H. J., Kawasawa, Y. I., Cheng, F., Zhu, Y., Xu, X., Li, M., et al. (2011). Spatio-temporal transcriptome of the human brain. Nature, 478(7370), 483–489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapranov, P., St Laurent, G., Raz, T., Ozsolak, F., Reynolds, C. P., Sorensen, P. H., et al. (2010). The majority of total nuclear-encoded non-ribosomal RNA in a human cell is’ dark matter’un-annotated RNA. BMC Biology, 8(1), 149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karp, X., & Ambros, V. (2005). Encountering microRNAs in cell fate signaling. Science, 310(5752), 1288–1289.

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki, H., & Taira, K. (2003). Hes1 is a target of microRNA-23 during retinoic-acid-induced neuronal differentiation of NT2 cells. Nature, 423(6942), 838–842.

    Article  CAS  PubMed  Google Scholar 

  • Kawase-Koga, Y., Low, R., Otaegi, G., Pollock, A., Deng, H., Eisenhaber, F., et al. (2010). RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cells. Journal of Cell Science, 123(4), 586–594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawase-Koga, Y., Otaegi, G., & Sun, T. (2009). Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Developmental Dynamics, 238(11), 2800–2812.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiecker, C., & Lumsden, A. (2005). Compartments and their boundaries in vertebrate brain development. Nature Reviews Neuroscience, 6(7), 553.

    Article  CAS  PubMed  Google Scholar 

  • Kim, V. N. (2005). MicroRNA biogenesis: Coordinated cropping and dicing. Nature Reviews Molecular Cell Biology, 6(5), 376–385.

    Article  CAS  PubMed  Google Scholar 

  • Kloosterman, W. P., Wienholds, E., de Bruijn, E., Kauppinen, S., & Plasterk, R. H. (2006). In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nature Methods, 3(1), 27–29.

    Article  CAS  PubMed  Google Scholar 

  • Kole, A. J., Swahari, V., Hammond, S. M., & Deshmukh, M. (2011). miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes & Development, 25(2), 125–130.

    Article  CAS  Google Scholar 

  • Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., et al. (2005). Combinatorial microRNA target predictions. Nature Genetics, 37(5), 495–500.

    Article  CAS  PubMed  Google Scholar 

  • Krichevsky, A. M., King, K. S., Donahue, C. P., Khrapko, K., & Kosik, K. S. (2003). A microRNA array reveals extensive regulation of microRNAs during brain development. RNA, 9(10), 1274–1281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krichevsky, A. M., Sonntag, K. C., Isacson, O., & Kosik, K. S. (2006). Specific microRNAs modulate embryonic stem cell–derived neurogenesis. Stem Cells, 24(4), 857–864.

    Article  CAS  PubMed  Google Scholar 

  • Le, M. T., Xie, H., Zhou, B., Chia, P. H., Rizk, P., Um, M., et al. (2009). MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Molecular and Cellular Biology, 29(19), 5290–5305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75(5), 843–854.

    Article  CAS  PubMed  Google Scholar 

  • Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G.-J., Kennerdell, J. R., et al. (2012). The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature, 482(7386), 519–523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, C., & Zhao, X. (2009). MicroRNAs in adult and embryonic neurogenesis. NeuroMolecular Medicine, 11(3), 141–152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loring, J., Wen, X., Lee, J., Seilhamer, J., & Somogyi, R. (2001). A gene expression profile of Alzheimer’s disease. DNA and Cell Biology, 20(11), 683–695.

    Article  CAS  PubMed  Google Scholar 

  • Lu, M., Jolly, M. K., Levine, H., Onuchic, J. N., & Ben-Jacob, E. (2013). MicroRNA-based regulation of epithelial–hybrid–mesenchymal fate determination. Proceedings of the National Academy of Sciences, 110(45), 18144–18149.

    Article  Google Scholar 

  • Lukiw, W. J. (2013). Circular RNA (circRNA) in Alzheimer’s disease (AD). Frontiers in Genetics, 4, 307.

    PubMed  PubMed Central  Google Scholar 

  • Luxenhofer, G., Helmbrecht, M. S., Langhoff, J., Giusti, S. A., Refojo, D., & Huber, A. B. (2014). MicroRNA-9 promotes the switch from early-born to late-born motor neuron populations by regulating Onecut transcription factor expression. Developmental Biology, 386(2), 358–370.

    Article  CAS  PubMed  Google Scholar 

  • Makeyev, E. V., Zhang, J., Carrasco, M. A., & Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell, 27(3), 435–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattick, J. S. (2001). Non-coding RNAs: The architects of eukaryotic complexity. EMBO Reports, 2(11), 986–991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattick, J. S., & Makunin, I. V. (2006). Non-coding RNA. Human Molecular Genetics, 15((suppl_1)), R17–R29.

    Article  CAS  PubMed  Google Scholar 

  • Miyoshi, N., Ishii, H., Nagano, H., Haraguchi, N., Dewi, D. L., Kano, Y., et al. (2011). Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell, 8(6), 633–638.

    Article  CAS  PubMed  Google Scholar 

  • Motti, D., Bixby, J. L., & Lemmon, V. P. (2012). MicroRNAs and neuronal development. Seminars in Fetal and Neonatal Medicine, 17(6), 347–352.

    Article  PubMed  Google Scholar 

  • Muljo, S. A., Kanellopoulou, C., & Aravind, L. (2010). MicroRNA targeting in mammalian genomes: genes and mechanisms. Wiley Interdisciplinary Reviews: Systems Biology and Medicine, 2(2), 148–161.

    CAS  PubMed  Google Scholar 

  • Narendra, D., Tanaka, A., Suen, D.-F., & Youle, R. J. (2009). Parkin-induced mitophagy in the pathogenesis of Parkinson disease. Autophagy, 5(5), 706–708.

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V., & Mendell, J. T. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 435(7043), 839–843.

    Article  CAS  PubMed  Google Scholar 

  • Otto, T., Candido, S. V., Pilarz, M. S., Sicinska, E., Bronson, R. T., Bowden, M., et al. (2017). Cell cycle-targeting microRNAs promote differentiation by enforcing cell-cycle exit. Proceedings of the National Academy of Sciences, 114(40), 10660–10665.

    Article  CAS  Google Scholar 

  • Pandey, A., Jauhari, A., Singh, T., Singh, P., Singh, N., Srivastava, A. K., et al. (2015a). Transactivation of P53 by cypermethrin induced miR-200 and apoptosis in neuronal cells. Toxicology Research, 4(6), 1578–1586.

    Article  CAS  Google Scholar 

  • Pandey, A., Singh, P., Jauhari, A., Singh, T., Khan, F., Pant, A. B., et al. (2015b). Critical role of the miR-200 family in regulating differentiation and proliferation of neurons. Journal of Neurochemistry, 133(5), 640–652.

    Article  CAS  PubMed  Google Scholar 

  • Peng, C., Li, N., Ng, Y.-K., Zhang, J., Meier, F., Theis, F. J., et al. (2012). A unilateral negative feedback loop between miR-200 microRNAs and Sox2/E2F3 controls neural progenitor cell-cycle exit and differentiation. The Journal of Neuroscience, 32(38), 13292–13308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, D., Wang, H., Li, L., Ma, X., Chen, Y., Zhou, H., et al. (2018). miR-34c-5p promotes eradication of acute myeloid leukemia stem cells by inducing senescence through selective RAB27B targeting to inhibit exosome shedding. Leukemia, 32, 1180.

    Article  CAS  PubMed  Google Scholar 

  • Petri, R., Malmevik, J., Fasching, L., Åkerblom, M., & Jakobsson, J. (2014). miRNAs in brain development. Experimental Cell Research, 321(1), 84–89.

    Article  CAS  PubMed  Google Scholar 

  • Qi, X. (2015). The role of miR-9 during neuron differentiation of mouse retinal stem cells. Artificial Cells, Nanomedicine, and Biotechnology. https://doi.org/10.3109/21691401.2015.1111231.

    Article  PubMed  Google Scholar 

  • Rajewsky, N. (2006). microRNA target predictions in animals. Nature Genetics, 38, S8–S13.

    Article  CAS  PubMed  Google Scholar 

  • Roese-Koerner, B., Stappert, L., Berger, T., Braun, N. C., Veltel, M., Jungverdorben, J., et al. (2016). Reciprocal regulation between bifunctional miR-9/9∗ and its transcriptional modulator notch in human neural stem cell self-renewal and differentiation. Stem Cell Reports, 7(2), 207–219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roshan, R., Shridhar, S., Sarangdhar, M. A., Banik, A., Chawla, M., Garg, M., et al. (2014). Brain-specific knockdown of miR-29 results in neuronal cell death and ataxia in mice. RNA, 20(8), 1287–1297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandberg, R., Yasuda, R., Pankratz, D. G., Carter, T. A., Del Rio, J. A., Wodicka, L., et al. (2000). Regional and strain-specific gene expression mapping in the adult mouse brain. Proceedings of the National Academy of Sciences, 97(20), 11038–11043.

    Article  CAS  Google Scholar 

  • Santra, M., Chopp, M., Santra, S., Nallani, A., Vyas, S., Zhang, Z. G., et al. (2016). Thymosin beta 4 up-regulates miR-200a expression and induces differentiation and survival of rat brain progenitor cells. Journal of Neurochemistry, 136(1), 118–132.

    Article  PubMed  Google Scholar 

  • Sayed, D., & Abdellatif, M. (2011). MicroRNAs in development and disease. Physiological Reviews, 91(3), 827–887.

    Article  CAS  PubMed  Google Scholar 

  • Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature, 439(7074), 283–289.

    Article  CAS  PubMed  Google Scholar 

  • Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., & Ambros, V. (2004). Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biology, 5(3), R13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shin, S., & Blenis, J. (2010). ERK2/Fra1/ZEB pathway induces epithelial-to-mesenchymal transition. Routledge: Taylor & Francis.

    Book  Google Scholar 

  • Shin, J., Shin, Y., Oh, S., Yang, H., Yu, W., Lee, J., et al. (2014). MiR-29b controls fetal mouse neurogenesis by regulating ICAT-mediated Wnt/β-catenin signaling. Cell Death & Disease, 5(10), e1473.

    Article  CAS  Google Scholar 

  • Siemens, H., Jackstadt, R., Hünten, S., Kaller, M., Menssen, A., Götz, U., et al. (2011). miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle, 10(24), 4256–4271.

    Article  CAS  PubMed  Google Scholar 

  • Sim, S.-E., Lim, C.-S., Kim, J.-I., Seo, D., Chun, H., Yu, N.-K., et al. (2016). The brain-enriched MicroRNA miR-9-3p regulates synaptic plasticity and memory. The Journal of Neuroscience, 36(33), 8641–8652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, T., Jauhari, A., Pandey, A., Singh, P., B Pant, A., Parmar, D., et al. (2014). Regulatory triangle of neurodegeneration, adult neurogenesis and microRNAs. CNS & Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders), 13(1), 96–103.

    Google Scholar 

  • Stefani, G., & Slack, F. J. (2008). Small non-coding RNAs in animal development. Nature Reviews Molecular Cell Biology, 9(3), 219.

    Article  CAS  PubMed  Google Scholar 

  • Tanzer, A., & Stadler, P. F. (2004). Molecular evolution of a microRNA cluster. Journal of Molecular Biology, 339(2), 327–335.

    Article  CAS  PubMed  Google Scholar 

  • Tau, G. Z., & Peterson, B. S. (2010). Normal development of brain circuits. Neuropsychopharmacology, 35(1), 147.

    Article  PubMed  Google Scholar 

  • Terasawa, K., Ichimura, A., Sato, F., Shimizu, K., & Tsujimoto, G. (2009). Sustained activation of ERK1/2 by NGF induces microRNA-221 and 222 in PC12 cells. FEBS Journal, 276(12), 3269–3276.

    Article  CAS  PubMed  Google Scholar 

  • Tremblay, R. G., Sikorska, M., Sandhu, J. K., Lanthier, P., Ribecco-Lutkiewicz, M., & Bani-Yaghoub, M. (2010). Differentiation of mouse Neuro 2A cells into dopamine neurons. Journal of Neuroscience Methods, 186(1), 60–67.

    Article  CAS  PubMed  Google Scholar 

  • Visvanathan, J., Lee, S., Lee, B., Lee, J. W., & Lee, S.-K. (2007). The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes & Development, 21(7), 744–749.

    Article  CAS  Google Scholar 

  • Wang, Z.-M., Du, W.-J., Piazza, G. A., & Xi, Y. (2013). MicroRNAs are involved in the self-renewal and differentiation of cancer stem cells. Acta Pharmacologica Sinica, 34(11), 1374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheeler, B. M., Heimberg, A. M., Moy, V. N., Sperling, E. A., Holstein, T. W., Heber, S., et al. (2009). The deep evolution of metazoan microRNAs. Evolution & Development, 11(1), 50–68.

    Article  CAS  Google Scholar 

  • Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., de Bruijn, E., et al. (2005). MicroRNA expression in zebrafish embryonic development. Science, 309(5732), 310–311.

    Article  CAS  PubMed  Google Scholar 

  • Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E., & Plasterk, R. H. (2003). The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nature Genetics, 35(3), 217–218.

    Article  CAS  PubMed  Google Scholar 

  • Wienholds, E., & Plasterk, R. H. (2005). MicroRNA function in animal development. FEBS Letters, 579(26), 5911–5922.

    Article  CAS  PubMed  Google Scholar 

  • Xie, H.-R., Hu, L.-S., & Li, G.-Y. (2010). SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson’s disease. Chinese Medical Journal, 123(8), 1086–1092.

    CAS  PubMed  Google Scholar 

  • Xue, Q., Yu, C., Wang, Y., Liu, L., Zhang, K., Fang, C., et al. (2016). miR-9 and miR-124 synergistically affect regulation of dendritic branching via the AKT/GSK3β pathway by targeting Rap2a. Scientific Reports, 6, 26781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav, S., Jauhari, A., Singh, N., Singh, T., Srivastav, A. K., Singh, P., et al. (2015). MicroRNAs are emerging as most potential molecular biomarkers. Biochemistry & Analytical Biochemistry. https://doi.org/10.4172/2161-1009.1000191.

    Article  Google Scholar 

  • Yadav, S., Pandey, A., Shukla, A., Talwelkar, S. S., Kumar, A., Pant, A. B., et al. (2011). miR-497 and miR-302b regulate ethanol-induced neuronal cell death through BCL2 protein and cyclin D2. Journal of Biological Chemistry, 286(43), 37347–37357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, S., Toledo, E. M., Rosmaninho, P., Peng, C., Uhlén, P., Castro, D. S., et al. (2018). A Zeb2-miR-200c loop controls midbrain dopaminergic neuron neurogenesis and migration. Communications Biology, 1(1), 75. https://doi.org/10.1038/s42003-018-0080-0.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao, C.-X., Wei, Q.-X., Zhang, Y.-Y., Wang, W.-P., Xue, L.-X., Yang, F., et al. (2013). miR-200b targets GATA-4 during cell growth and differentiation. RNA Biology, 10(4), 465–480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, J.-Y., Chung, K.-H., Deo, M., Thompson, R. C., & Turner, D. L. (2008). MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Experimental Cell Research, 314(14), 2618–2633.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, G.-Y., Wang, J., Jia, Y.-J., Han, R., Li, P., & Zhu, D.-N. (2015). MicroRNA-9 promotes the neuronal differentiation of rat bone marrow mesenchymal stem cells by activating autophagy. Neural Regeneration Research, 10(2), 314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou, Y., Huang, Y., Yang, J., Wu, J., & Luo, C. (2017). miR-34a is downregulated in human osteosarcoma stem-like cells and promotes invasion, tumorigenic ability and self-renewal capacity. Molecular Medicine Reports, 15(4), 1631–1637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Funding for the work carried out in the present study has been provided by CSIR network projects (Grant Nos. BSC0111, BSC0115). Mr. Abhishek Jauhari is grateful to UGC, New Delhi, for providing research fellowship. The CSIR-IITR communication reference number is 3426.

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Jauhari, A., Yadav, S. MiR-34 and MiR-200: Regulator of Cell Fate Plasticity and Neural Development. Neuromol Med 21, 97–109 (2019). https://doi.org/10.1007/s12017-019-08535-9

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