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MicroRNAs tell an evo–devo story

Abstract

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Evolutionary developmental biology, often called evo–devo, seeks to understand the ancestral relationship among organisms by comparing their developmental strategies and ultimately reconstructing the pathways that led to the extraordinary variety of biological forms. The insights from this synthesis of developmental biology and evolutionary principles are useful for understanding the development of the nervous system. The pervasive and crucial roles of microRNAs in nervous system development suggest that these short non-coding transcripts deserve a chapter in the unfolding evo–devo story. The structure of microRNAs, their physical proximity to other genes and their network effects on targets make this class of transcripts tractable genetic material for evolutionary change.

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Figure 1: RNA network structure.
Figure 2: MicroRNA numbers among representative species.
Figure 3: The evolution of a microRNA.

References

  1. Kosik, K. S. The neuronal microRNA system. Nature Rev. Neurosci. 7, 911–992 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906 (2000).

    CAS  Google Scholar 

  4. Giraldez, A. J. et al. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75–79 (2006).

    Article  CAS  Google Scholar 

  5. Miller, G. On the origins of the nervous system. Science 325, 24–26 (2009).

    Article  CAS  Google Scholar 

  6. Sakarya, O. et al. A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2, e506 (2007).

    Article  Google Scholar 

  7. Davidson, E. H. & Erwin, D. H. Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800 (2006).

    Article  CAS  Google Scholar 

  8. Yekta, S., Shih, I. H. & Bartel, D. P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594–596 (2004).

    Article  CAS  Google Scholar 

  9. Winter, J., Jung, S., Keller, S., Gregory, R. I. & Diederichs, S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nature Cell Biol. 11, 228–234 (2009).

    Article  CAS  Google Scholar 

  10. Sempere, L. F., Cole, C. N., McPeek, M. A. & Peterson, K. J. The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J. Exp. Zool. B Mol. Dev. Evol. 306, 575–588 (2006).

    Article  Google Scholar 

  11. Okamura, K. et al. The regulatory activity of microRNA* species has substantial influence on microRNA and 30′ UTR evolution. Nature Struct. Mol. Biol. 15, 354–363 (2008).

    Article  CAS  Google Scholar 

  12. Wheeler, B. M. et al. The deep evolution of metazoan microRNAs. Evol. Dev. 11, 50–68 (2009).

    Article  CAS  Google Scholar 

  13. Giraldez, A. J. et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833–838 (2005).

    Article  CAS  Google Scholar 

  14. Sokol, N. S. & Ambros, V. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev. 19, 2343–2354 (2005).

    Article  CAS  Google Scholar 

  15. Brennecke, J., Stark, A. & Cohen, S. M. Not miR-ly muscular: microRNAs and muscle development. Genes Dev. 19, 2261–2264 (2005).

    Article  CAS  Google Scholar 

  16. Lim, L. et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769–773 (2005).

    Article  CAS  Google Scholar 

  17. Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).

    Article  CAS  Google Scholar 

  18. Papagiannakopoulos, T., Shapiro, A. & Kosik, K. S. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 68, 8164–8172 (2008).

    Article  CAS  Google Scholar 

  19. Chi, S. W., Zang, J. B., Mele, A. & Darnell, R. B. Argonaute HITS-CLIP decodes microRNA–mRNA interaction maps. Nature 460, 479–486 (2009).

    Article  CAS  Google Scholar 

  20. Umulis, D. M., Serpe, M., O'Connor, M. B. & Othmer, H. G. Robust, bistable patterning of the dorsal surface of the Drosophila embryo. Proc. Natl Acad. Sci. USA 103, 11613–11618 (2006).

    Article  CAS  Google Scholar 

  21. Wang, Y. C. & Ferguson, E. L. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434, 229–234 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Berezikov, E. et al. Diversity of microRNAs in human and chimpanzee brain. Nature Genet. 38, 1375–1377 (2006).

    Article  CAS  Google Scholar 

  24. Hallam, S. J. & Jin, Y. lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans. Nature 395, 78–82 (1998).

    Article  CAS  Google Scholar 

  25. Lin, S. Y. et al. The C. elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell 4, 639–650 (2003).

    Article  CAS  Google Scholar 

  26. Abrahante, J. E. et al. The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev. Cell 4, 625–637 (2003).

    Article  CAS  Google Scholar 

  27. Gierer, A. & Meinhardt, H. A theory of biological pattern formation. Kybernetik 12, 30–39 (1972).

    Article  CAS  Google Scholar 

  28. Singh, N. P. & Mishra, R. K. A double-edged sword to force posterior dominance of Hox genes. Bioessays 30, 1058–1061 (2008).

    Article  CAS  Google Scholar 

  29. Yekta, S., Tabin, C. J. & Bartel, D. P. MicroRNAs in the Hox network: an apparent link to posterior prevalence. Nature Rev. Genet. 9, 789–796 (2008).

    Article  CAS  Google Scholar 

  30. Chang, S., Johnston, R. J. Jr, Frokjaer-Jensen, C., Lockery, S. & Hobert, O. MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430, 785–789 (2004).

    Article  CAS  Google Scholar 

  31. Chang, S., Johnston, R. J. Jr & Hobert, O. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17, 2123–2137 (2003).

    Article  CAS  Google Scholar 

  32. Johnston, R. J. & Hobert, O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426, 845–849 (2003).

    Article  CAS  Google Scholar 

  33. Johnston, R. J. Jr, Chang, S., Etchberger, J. F., Ortiz, C. O. & Hobert, O. MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl. Acad. Sci. USA 102, 12449–12454 (2005).

    Article  CAS  Google Scholar 

  34. Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J. A. & Kosik, K. S. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137, 647–658 (2009).

    Article  CAS  Google Scholar 

  35. Justman, Q. A., Serber, Z., Ferrell, J. E. Jr, El-Samad, H. & Shokat, K. M. Tuning the activation threshold of a kinase network by nested feedback loops. Science 324, 509–512 (2009).

    Article  CAS  Google Scholar 

  36. Choi, P. S. et al. Members of the miRNA-200 family regulate olfactory neurogenesis. Neuron 57, 41–55 (2008).

    Article  CAS  Google Scholar 

  37. Jan, Y. N. & Jan, L. Y. Neronal cell fate specification in Drosophila. Curr. Opin. Neurobiol. 4, 8–13 (1994).

    Article  CAS  Google Scholar 

  38. Hobert, O. Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc. Natl Acad. Sci. USA 105, 20067–20071 (2008).

    Article  CAS  Google Scholar 

  39. Conaco, C., Otto, S., Han, J. J. & Mandel, G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl Acad. Sci. USA 103, 2422–2427 (2006).

    Article  CAS  Google Scholar 

  40. Hornstein, E. & Shomron, N. Canalization of development by microRNAs. Nature Genet. 38, S20–S24 (2006).

    Article  CAS  Google Scholar 

  41. Schratt, G. M. et al. A brain-specific microRNA regulates dendritic spine development. Nature 439, 283–289 (2006).

    Article  CAS  Google Scholar 

  42. Lisman, J. Actin's actions in LTP-induced synapse growth. Neuron 38, 361–362 (2003).

    Article  CAS  Google Scholar 

  43. Siegel, G. et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nature Cell Biol. 11, 705–716 (2009).

    Article  CAS  Google Scholar 

  44. Kang, R. et al. Neural palmitoyl-proteomics reveals dynamic synaptic palmitoylation. Nature 456, 904–909 (2008).

    Article  CAS  Google Scholar 

  45. Jones, T. L., Degtyarev, M. Y. & Backlund, P. S. Jr. The stoichiometry of Gαs palmitoylation in its basal and activated states. Biochemistry 36, 7185–7191 (1997).

    Article  CAS  Google Scholar 

  46. Buhl, A. M., Johnson, N. L., Dhanasekaran, N. & Johnson, G. L. Gα12 and Gα13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631–24634 (1995).

    Article  CAS  Google Scholar 

  47. Vo, N. et al. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl Acad. Sci. USA 102, 16426–16431 (2005).

    Article  CAS  Google Scholar 

  48. Nudelman, A. S. et al. Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 25 Jun 2009 (doi:10.1002/hipo.20646).

  49. Wayman, G. A. et al. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl Acad. Sci. USA 105, 9093–0908 (2008).

    Article  CAS  Google Scholar 

  50. Cheng, H. Y. et al. microRNA modulation of circadian-clock period and entrainment. Neuron 54, 813–829 (2007).

    Article  CAS  Google Scholar 

  51. Larroux, C. et al. Genesis and expansion of metazoan transcription factor gene classes. Mol. Biol. Evol. 25, 980–996 (2008).

    Article  CAS  Google Scholar 

  52. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009).

    Article  CAS  Google Scholar 

  53. Berezikov, E. et al. Diversity of microRNAs in human and chimpanzee brain. Nature Genet. 38, 1375–1377 (2006).

    Article  CAS  Google Scholar 

  54. Liang, H. & Li, W. H. Lowly expressed human microRNA genes evolve rapidly. Mol. Biol. Evol. 26, 1195–1198 (2009).

    Article  CAS  Google Scholar 

  55. King, M. C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).

    Article  CAS  Google Scholar 

  56. Taft, R. J., Pheasant, M. & Mattick, J. S. The relationship between non-protein-coding DNA and eukaryotic complexity. Bioessays 29, 288–299 (2007).

    Article  CAS  Google Scholar 

  57. Heimberg, A. M., Sempere, L. F., Moy, V. N., Donoghue, P. C. & Peterson, K. J. MicroRNAs and the advent of vertebrate morphological complexity. Proc. Natl Acad. Sci USA 105, 2946–2950 (2008).

    Article  CAS  Google Scholar 

  58. Kirschner, M. & Gerhart, J. Evolvability. Proc. Natl Acad. Sci. USA 95, 8420–8427 (1998).

    Article  CAS  Google Scholar 

  59. Chen, K. & Rajewsky, N. The evolution of gene regulation by transcription factors and microRNAs. Nature Rev. Genet. 8, 93–103 (2007).

    Article  CAS  Google Scholar 

  60. Liu, N. et al. The evolution and functional diversification of animal microRNA genes. Cell Res. 18, 985–996 (2008).

    Article  CAS  Google Scholar 

  61. Bartel, D. P. & Chen, C. Z. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nature Rev. Genet. 5, 396–400 (2004).

    Article  CAS  Google Scholar 

  62. Griffiths-Jones, S., Saini, H. K., van Dongen, S. & Enright, A. J. miRBase: tools for microRNA genomics Nucleic Acids Res. 36, D154–D158 (2008).

    Article  CAS  Google Scholar 

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Acknowledgements

I thank the members of the Kosik laboratory, B. Shraiman and N. Shomron for their comments and suggestions. C. Conaco prepared the original figure 2.

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Kosik, K. MicroRNAs tell an evo–devo story. Nat Rev Neurosci 10, 754–759 (2009). https://doi.org/10.1038/nrn2713

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