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

  • Abhishek Jauhari
  • Sanjay YadavEmail author
Review Paper
  • 95 Downloads

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.

Keywords

MicroRNAs Cell fate Brain development Differentiation MiR-34 and miR-200 

Notes

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.

Compliance with Ethical Standards

Conflict of interest

There is no conflict of interest regarding the publication of this review article.

References

  1. Aberdam, D., Candi, E., Knight, R. A., & Melino, G. (2008). miRNAs, ‘stemness’ and skin. Trends in Biochemical Sciences, 33(12), 583–591.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. Alvarez-Garcia, I., & Miska, E. A. (2005). MicroRNA functions in animal development and human disease. Development, 132(21), 4653–4662.CrossRefPubMedGoogle Scholar
  4. Amaral, P. P., & Mattick, J. S. (2008). Noncoding RNA in development. Mammalian Genome, 19(7–8), 454–492.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Andersen, S. L. (2003). Trajectories of brain development: point of vulnerability or window of opportunity? Neuroscience and Biobehavioral Reviews, 27(1), 3–18.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Axtell, M. J., & Bartel, D. P. (2005). Antiquity of microRNAs and their targets in land plants. The Plant Cell, 17(6), 1658–1673.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Azari, H., & Reynolds, B. A. (2016). In vitro models for neurogenesis. Cold Spring Harbor Perspectives in Biology, 8(6), a021279.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bartel, D. P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116(2), 281–297.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. Bhaskaran, M., & Mohan, M. (2014). MicroRNAs: History, biogenesis, and their evolving role in animal development and disease. Veterinary Pathology, 51(4), 759–774.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. Carleton, M., Cleary, M. A., & Linsley, P. S. (2007). MicroRNAs and cell cycle regulation. Cell Cycle, 6(17), 2127–2132.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. Chen, K., & Rajewsky, N. (2007). The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics, 8(2), 93–103.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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.
  26. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Coolen, M., & Bally-Cuif, L. (2009). MicroRNAs in brain development and physiology. Current Opinion in Neurobiology, 19(5), 461–470.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gangaraju, V. K., & Lin, H. (2009). MicroRNAs: Key regulators of stem cells. Nature Reviews Molecular Cell Biology, 10(2), 116.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Gao, F.-B. (2008). Posttranscriptional control of neuronal development by microRNA networks. Trends in Neurosciences, 31(1), 20–26.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedCentralGoogle Scholar
  42. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. He, X., & Rosenfeld, M. G. (1991). Mechanisms of complex transcriptional regulation: implications for brain development. Neuron, 7(2), 183–196.CrossRefPubMedGoogle Scholar
  49. Hermeking, H. (2010). The miR-34 family in cancer and apoptosis. Cell Death and Differentiation, 17(2), 193–199.CrossRefPubMedGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefPubMedGoogle Scholar
  52. 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.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. Huang, B., & Zhang, R. (2014). Regulatory non-coding RNAs: revolutionizing the RNA world. Molecular Biology Reports, 41(6), 3915–3923.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Hwang, H., & Mendell, J. (2006). MicroRNAs in cell proliferation, cell death, and tumorigenesis. British Journal of Cancer, 94(6), 776.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. 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.CrossRefPubMedGoogle Scholar
  60. 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.CrossRefPubMedGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. Kalluri, R., & Weinberg, R. A. (2009). The basics of epithelial-mesenchymal transition. The Journal of Clinical Investigation, 119(6), 1420–1428.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Karp, X., & Ambros, V. (2005). Encountering microRNAs in cell fate signaling. Science, 310(5752), 1288–1289.CrossRefPubMedGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Kiecker, C., & Lumsden, A. (2005). Compartments and their boundaries in vertebrate brain development. Nature Reviews Neuroscience, 6(7), 553.CrossRefPubMedGoogle Scholar
  70. Kim, V. N. (2005). MicroRNA biogenesis: Coordinated cropping and dicing. Nature Reviews Molecular Cell Biology, 6(5), 376–385.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefPubMedGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. 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.CrossRefPubMedGoogle Scholar
  74. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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.CrossRefPubMedGoogle Scholar
  76. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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.CrossRefPubMedGoogle Scholar
  78. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Liu, C., & Zhao, X. (2009). MicroRNAs in adult and embryonic neurogenesis. NeuroMolecular Medicine, 11(3), 141–152.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 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.CrossRefPubMedGoogle Scholar
  81. 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.CrossRefGoogle Scholar
  82. Lukiw, W. J. (2013). Circular RNA (circRNA) in Alzheimer’s disease (AD). Frontiers in Genetics, 4, 307.PubMedPubMedCentralGoogle Scholar
  83. 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.CrossRefPubMedGoogle Scholar
  84. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Mattick, J. S. (2001). Non-coding RNAs: The architects of eukaryotic complexity. EMBO Reports, 2(11), 986–991.CrossRefPubMedPubMedCentralGoogle Scholar
  86. Mattick, J. S., & Makunin, I. V. (2006). Non-coding RNA. Human Molecular Genetics, 15((suppl_1)), R17–R29.CrossRefPubMedGoogle Scholar
  87. 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.CrossRefPubMedGoogle Scholar
  88. Motti, D., Bixby, J. L., & Lemmon, V. P. (2012). MicroRNAs and neuronal development. Seminars in Fetal and Neonatal Medicine, 17(6), 347–352.CrossRefPubMedGoogle Scholar
  89. 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.PubMedGoogle Scholar
  90. 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.CrossRefPubMedGoogle Scholar
  91. 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.CrossRefPubMedGoogle Scholar
  92. 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.CrossRefGoogle Scholar
  93. 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.CrossRefGoogle Scholar
  94. 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.CrossRefPubMedGoogle Scholar
  95. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 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.CrossRefPubMedGoogle Scholar
  97. Petri, R., Malmevik, J., Fasching, L., Åkerblom, M., & Jakobsson, J. (2014). miRNAs in brain development. Experimental Cell Research, 321(1), 84–89.CrossRefPubMedGoogle Scholar
  98. 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.CrossRefPubMedGoogle Scholar
  99. Rajewsky, N. (2006). microRNA target predictions in animals. Nature Genetics, 38, S8–S13.CrossRefPubMedGoogle Scholar
  100. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 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.CrossRefGoogle Scholar
  103. 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.CrossRefPubMedGoogle Scholar
  104. Sayed, D., & Abdellatif, M. (2011). MicroRNAs in development and disease. Physiological Reviews, 91(3), 827–887.CrossRefPubMedGoogle Scholar
  105. 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.CrossRefPubMedGoogle Scholar
  106. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  107. Shin, S., & Blenis, J. (2010). ERK2/Fra1/ZEB pathway induces epithelial-to-mesenchymal transition. Routledge: Taylor & Francis.CrossRefGoogle Scholar
  108. 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.CrossRefGoogle Scholar
  109. 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.CrossRefPubMedGoogle Scholar
  110. 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.CrossRefPubMedGoogle Scholar
  111. 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
  112. Stefani, G., & Slack, F. J. (2008). Small non-coding RNAs in animal development. Nature Reviews Molecular Cell Biology, 9(3), 219.CrossRefPubMedGoogle Scholar
  113. Tanzer, A., & Stadler, P. F. (2004). Molecular evolution of a microRNA cluster. Journal of Molecular Biology, 339(2), 327–335.CrossRefPubMedGoogle Scholar
  114. Tau, G. Z., & Peterson, B. S. (2010). Normal development of brain circuits. Neuropsychopharmacology, 35(1), 147.CrossRefPubMedGoogle Scholar
  115. 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.CrossRefPubMedGoogle Scholar
  116. 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.CrossRefPubMedGoogle Scholar
  117. 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.CrossRefGoogle Scholar
  118. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 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.CrossRefGoogle Scholar
  120. 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.CrossRefPubMedGoogle Scholar
  121. 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.CrossRefPubMedGoogle Scholar
  122. Wienholds, E., & Plasterk, R. H. (2005). MicroRNA function in animal development. FEBS Letters, 579(26), 5911–5922.CrossRefPubMedGoogle Scholar
  123. 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.PubMedGoogle Scholar
  124. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 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.CrossRefGoogle Scholar
  126. 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.CrossRefPubMedGoogle Scholar
  127. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  129. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  130. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  131. 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.CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Developmental Toxicology Laboratory, Systems Toxicology and Health Risk Assessment GroupCSIR-Indian Institute of Toxicology Research (CSIR-IITR)LucknowIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)LucknowIndia
  3. 3.Neuroapoptosis Laboratory, Department of Neurological SurgeryUniversity of PittsburghPittsburghUSA

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