Evolution under canalization and the dual roles of microRNAs - A hypothesis

Genome Research

Volumn 19, Issue 5, 2009, Pages 734-743

  Wu, Chung I ^a,b,c   Shen, Yang ^b   Tang, Tian ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

3' UNTRANSLATED REGION; DROSOPHILA MELANOGASTER; EVOLUTION; GENE DELETION; GENE EXPRESSION; GENETIC TRANSFECTION; GENETIC VARIABILITY; HUMAN; NATURAL SELECTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

ANIMALS; DROSOPHILA; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; GENETIC SPECIATION; HUMANS; MICE; MICRORNAS; MODELS, GENETIC; PHENOTYPE; SELECTION (GENETICS);

EID: 66049153398     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.084640.108     Document Type: Review

References (88)

1. Alon, U. 2007. An introduction to systems biology: Design principles of biological circuits. Chapman & Hall/CRC, Boca Raton, FL.
2. Alvarez-Garcia, I. and Miska, E.A. 2005. MicroRNA functions in animal development and human disease. Development 132: 4653-4662.
3. Baek, D., Villen, J., Shin, C., Camargo, F.D., Gygi, S.P., and Bartel, D.P. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
4. Bartel, D.P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
5. Bartel, D.P. and Chen, C.Z. 2004. Micromanagers of gene expression: The potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5: 396-400.
6. Berezikov, E., Thuemmler, F., van Laake, L.W., Kondova, I., Bontrop, R., Cuppen, E., and Plasterk, R.H.A. 2006. Diversity of microRNAs in human and chimpanzee brain. Nat. Genet. 38: 1375-1377.
7. Bergman, A. and Siegal, M.L. 2003. Evolutionary capacitance as a general feature of complex gene networks. Nature 424: 549-552.
8. Brennecke, J., Stark, A., Russell, R.B., and Cohen, S.M. 2005. Principles of microRNA-target recognition. PLoS Biol. 3: 404-418. (Pubitemid 40605291)
9. Bushati, N. and Cohen, S.M. 2007. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 23: 175-205.
10. Carrington, J.C. and Ambros, V. 2003. Role of microRNAs in plant and animal development. Science 301: 336-338.
11. Chen, K. and Rajewsky, N. 2007. The evolution of gene regulation by transcription factors and microRNAs. Nat. Rev. Genet. 8: 93-103. (Pubitemid 46122839)
12. Choi, W.Y., Giraldez, A.J., and Schier, A.F. 2007. Target protectors reveal dampening and balancing of nodal agonist and antagonist by miR-430. Science 318: 271-274.
13. Ciliberti, S., Martin, O.C., and Wagner, A. 2007a. Innovation and robustness in complex regulatory gene networks. Proc. Natl. Acad. Sci. 104: 13591-13596. (Pubitemid 350003365)
14. Ciliberti, S., Martin, O.C., and Wagner, A. 2007b. Robustness can evolve gradually in complex regulatory gene networks with varying topology. PLoS Comput. Biol. 3: 164-173. (Pubitemid 46318378)
15. Cohen, S.M., Brennecke, J., and Stark, A. 2006. Denoising feedback loops by thresholding - a new role for microRNAs. Genes & Dev. 20: 2769-2772.
16. Cui, Q., Yu, Z., Purisima, E.O., and Wang, E. 2006. Principles of microRNA regulation of a human cellular signaling network. Mol. Syst. Biol. 2: 46. doi: 10.1038/msb4100089. (Pubitemid 46061065)
17. Cui, Q., Yu, Z., Purisima, E.O., and Wang, E. 2007. MicroRNA regulation and interspecific variation of gene expression. Trends Genet. 23: 372-375. (Pubitemid 47088006)
18. Darwin, C. 1859. On the origin of species by means of natural selection. Murray, London, UK.
19. Fahlgren, N., Howell, M.D., Kasschau, K.D., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., Law, T.F., Grant, S.R., Dangl, J.L., et al. 2007. High-throughput sequencing of Arabidopsis microRNAs: Evidence for frequent birth and death of MIRNA genes. PLoS One 2: e219. doi: 10.1371/journal.pone. 0000219.
20. Farh, K.K.H., Grimson, A., Jan, C., Lewis, B.P., Johnston, W.K., Lim, L.P., Burge, C.B., and Bartel, D.P. 2005. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310: 1817-1821.
21. Fay, J.C. and Wu, C.-I. 2003. Sequence divergence, functional constraint, and selection in protein evolution. Annu. Rev. Genomics Hum. Genet. 4: 213-235.
22. Fisher, R.A. 1930. The genetical theory of natural selection. Clarendon Press. Oxford, UK.
23. Grimson, A., Farh, K.K.H., Johnston, W.K., Garrett-Engele, P., Lim, L.P., and Bartel, D.P. 2007. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol. Cell 27: 91-105.
24. Grun, D., Wang, Y.L., Langenberger, D., Gunsalus, K.C., and Rajewsky, N. 2005. MicroRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 1: 51-66.
25. Hermisson, J. and Wagner, G.P. 2004. The population genetic theory of hidden variation and genetic robustness. Genetics 168: 2271-2284.
26. Hobert, O. 2004. Common logic of transcription factor and microRNA action. Trends Biochem. Sci. 29: 462-468. (Pubitemid 39158869)
27. Hobert, O. 2007. miRNAs play a tune. Cell 131: 22-24. (Pubitemid 47498545)
28. Hobert, O. 2008. Gene regulation by transcription factors and microRNAs. Science 319: 1785-1786.
29. Hornstein, E. and Shomron, N. 2006. Canalization of development by microRNAs. Nat. Genet. 38: S20-S24. (Pubitemid 43920939)
30. Hornstein, E., Mansfield, J.H., Yekta, S., Hu, J.K.H., Harfe, B.D., McManus, M.T., Baskerville, S., Bartel, D.P., and Tabin, C.J. 2005. The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 438: 671-674.
31. Kaern, M., Elston, T.C., Blake, W.J., and Collins, J.J. 2005. Stochasticity in gene expression: From theories to phenotypes. Nat. Rev. Genet. 6: 451-464.
32. Karres, J.S., Hilgers, V., Carrera, I., Treisman, J., and Cohen, S.M. 2007. The conserved microRNA miR-8 tunes atrophin levels to prevent neurodegeneration in Drosophila. Cell 131: 136-145.
33. Kennell, J.A., Gerin, I., MacDougald, O.A., and Cadigan, K.M. 2008. The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc. Natl. Acad. Sci. 105: 15417-15422.
34. Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U., and Segal, E. 2007. The role of site accessibility in microRNA target recognition. Nat. Genet. 39: 1278-1284. (Pubitemid 47482690)
35. Krek, A., Grun, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein, E.J., MacMenamin, P., da Piedade, I., Gunsalus, K.C., Stoffel, M., et al. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37: 495-500.
36. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. 2001. Identification of novel genes coding for small expressed RNAs. Science 294: 853-858.
37. Lau, N.C., Lim, L.P., Weinstein, E.G., and Bartel, D.P. 2001. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294: 858-862.
38. Lee, R.C. and Ambros, V. 2001. An extensive class of small RNAs in Caenorhabditis elegans. Science 294: 862-864.
39. Lee, R.C., Feinbaum, R.L., and Ambros, V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
40. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P., and Burge, C.B. 2003. Prediction of mammalian microRNA targets. Cell 115: 787-798.
41. Lewis, B.P., Burge, C.B., and Bartel, D.P. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
42. Li, X. and Carthew, R.W. 2005. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123: 1267-1277.
43. Li, Y., Wang, F., Lee, J.A., and Gao, F.B. 2006. MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes & Dev. 20: 2793-2805.
44. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S., and Johnson, J.M. 2005. Microarray analysis shows that some microRNAs down-regulate large numbers of target mRNAs. Nature 433: 769-773.
45. Linsley, P.S., Schelter, J., Burchard, J., Kibukawa, M., Martin, M.M., Bartz, S.R., Johnson, J.M., Cummins, J.M., Raymond, C.K., Dai, H.Y., et al. 2007. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol. 27: 2240-2252.
46. Lu, J., Fu, Y.G., Kumar, S., Shen, Y., Zeng, K., Xu, A.L., Carthew, R., and Wu, C.-I. 2008a. Adaptive evolution of newly emerged micro-RNA genes in Drosophila. Mol. Biol. Evol. 25: 929-938.
47. Lu, J., Shen, Y., Wu, Q., Kumar, S., He, B., Shi, S., Carthew, R.W., Wang, S.M., and Wu, C.-I. 2008b. The birth and death of microRNA genes in Drosophila. Nat. Genet. 40: 351-355.
48. Makeyev, E.V. and Maniatis, T. 2008. Multilevel regulation of gene expression by microRNAs. Science 319: 1789-1790.
49. Marson, A., Levine, S.S., Cole, M.F., Frampton, G.M., Brambrink, T., Johnstone, S., Guenther, M.G., Johnston, W.K., Wernig, M., Newman, J., et al. 2008. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533.
50. Martinez, N.J., Ow, M.C., Barrasa, M.I., Hammell, M., Sequerra, R., Doucette-Stamm, L., Roth, F.P., Ambros, V.R., and Walhout, A.J.M. 2008. A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes & Dev. 22: 2535-2549.
51. Mehta, P., Goyal, S., and Wingreen, N.S. 2008. A quantitative comparison of sRNA-based and protein-based gene regulation. Mol. Syst. Biol. 4: 221. doi: 10.1038/msb.2008.58.
52. Meir, E., von Dassow, G., Munro, E., and Odell, G.M. 2002. Robustness, flexibility, and the role of lateral inhibition in the neurogenic network. Curr. Biol. 12: 778-786.
53. Miska, E.A., Alvarez-Saavedra, E., Abbott, A.L., Lau, N.C., Hellman, A.B., McGonagle, S.M., Bartel, D.P., Ambros, V.R., and Horvitz, H.R. 2007. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet. 3: 2395-2403.
54. Nakahara, K., Kim, K., Sciulli, C., Dowd, S.R., Minden, J.S., and Carthew, R.W. 2005. Targets of microRNA regulation in the Drosophila oocyte proteorne. Proc. Natl. Acad. Sci. 102: 12023-12028. (Pubitemid 41291122)
55. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V., and Mendell, J.T. 2005. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435: 839-843. (Pubitemid 40839736)
56. Ohta, T. 1973. Slightly deleterious mutant substitutions in evolution. Nature 246: 96-98.
57. Plasterk, R.H.A. 2006. MicroRNAs in animal development. Cell 124: 877-881.
58. Rajewsky, N. 2006. MicroRNA target predictions in animals. Nat. Genet. 38: S8-S13. (Pubitemid 43920937)
59. Raser, J.M. and O'Shea, E.K. 2005. Noise in gene expression: Origins, consequences, and control. Science 309: 2010-2013.
60. Rehwinkel, J., Natalin, P., Stark, A., Brennecke, J., Cohen, S.M., and Izaurralde, E. 2006. Genome-wide analysis of mRNAs regulated by Drosha and Argonaute proteins in Drosophila melanogaster. Mol. Cell. Biol. 26: 2965-2975.
61. Rendel, J.M. 1967. Canalization and gene control. Logos Press, London, UK.
62. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P. 2002. Prediction of plant microRNA targets. Cell 110: 513-520.
63. Rutherford, S.L. and Lindquist, S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396: 336-342.
64. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E.E., Nitsch, R., and Wulczyn, F.G. 2008. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 10: 987-993.
65. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
66. Sempere, L.F., Cole, C.N., McPeek, M.A., and Peterson, K.J. 2006. The phylogenetic distribution of metazoan microRNAs: Insights into evolutionary complexity and constraint. J. Exp. Zoolog. B Mol. Dev. Evol. 306: 575-588.
67. Siegal, M.L. and Bergman, A. 2002. Waddington's canalization revisited: Developmental stability and evolution. Proc. Natl. Acad. Sci. 99: 10528-10532.
68. Stark, A., Brennecke, J., Russell, R.B., and Cohen, S.M. 2003. Identification of Drosophila microRNA targets. PLoS Biol. 1: 397-409. (Pubitemid 39112138)
69. Stark, A., Brennecke, J., Bushati, N., Russell, R.B., and Cohen, S.M. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3′ UTR evolution. Cell 123: 1133-1146. (Pubitemid 41785426)
70. Stark, A., Lin, M.F., Kheradpour, P., Pedersen, J.S., Parts, L., Carlson, J.W., Crosby, M.A., Rasmussen, M.D., Roy, S., Deoras, A.N., et al. 2007. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 450: 219-232.
71. Stefani, G. and Slack, F.J. 2008. Small non-coding RNAs in animal development. Nat. Rev. Mol. Cell Biol. 9: 219-230.
72. Sullivan, C.S. 2008. New roles for large and small viral RNAs in evading host defences. Nat. Rev. Genet. 9: 503-507.
73. Sylvestre, Y., De Guire, V., Querido, E., Mukhopadhyay, U.K., Bourdeau, V., Major, F., Ferbeyre, G., and Chartrand, P. 2007. An E2F/miR-20a autoregulatory feedback loop. J. Biol. Chem. 282: 2135-2143.
74. Tsai, T.Y., Choi, Y.S., Ma, W., Pomerening, J.R., Tang, C., and Ferrell Jr., J.E. 2008. Robust, tunable biological oscillations from interlinked positive and negative feedback loops. Science 321: 126-129.
75. Tsang, J., Zhu, J., and van Oudenaarden, A. 2007. MicroRNA-mediated feedback and feed-forward loops are recurrent network motifs in mammals. Mol. Cell 26: 753-767. (Pubitemid 46856248)
76. Varghese, J. and Cohen, S.M. 2007. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes & Dev. 21: 2277-2282. (Pubitemid 47443333)
77. von Dassow, G., Meir, E., Munro, E.M., and Odell, G.M. 2000. The segment polarity network is a robust development module. Nature 406: 188-192.
78. Waddington, C.H. 1942. Analization of development and the inheritance of acquired characters. Nature 150: 563-565.
79. Waddington, C.H. 1959. Canalization of development and genetic assimilation of acquired characters. Nature 183: 1654-1655.
80. Wagner, A. 2005. Circuit topology and the evolution of robustness in two-gene circadian oscillators. Proc. Natl. Acad. Sci. 102: 11775-11780. (Pubitemid 41170801)
81. Wang, E. 2008. MicroRNA systems biology. In RNA technologies in cardiovascular medicine and research (eds. V.A. Erdmann et al.), pp. 69-86. Springer, Berlin-Heidelberg, Germany.
82. Wang, H.Y., Fu, Y.G., McPeek, M.S., Lu, X.M., Nuzhdin, S., Xu, A.L., Lu, J., Wu, M.L., and Wu, C.-I. 2008. Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions. Proc. Natl. Acad. Sci. 105: 6362-6367.
83. Wienholds, E. and Plasterk, R.H.A. 2005. MicroRNA function in animal development. FEBS Lett. 579: 5911-5922. (Pubitemid 41487106)
84. Wightman, B., Ha, I., and Ruvkun, G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern-formation in C. elegans. Cell 75: 855-862.
85. Woods, K., Thomson, J.M., and Hammond, S.M. 2007. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J. Biol. Chem. 282: 2130-2134. (Pubitemid 47076737)
86. Wu, C.-I. and Palopoli, M.F. 1994. Genetics of postmating reproductive isolation in animals. Annu. Rev. Genet. 28: 283-308.
87. Wu, C.-I. and Ting, C.T. 2004. Genes and speciation. Nat. Rev. Genet. 5: 114-122. (Pubitemid 38160278)
88. Xiao, C.C., Calado, D.P., Galler, G., Thai, T.H., Patterson, H.C., Wang, J., Rajewsky, N., Bender, T.P., and Rajewsky, K. 2007. MiR-150 controls B cell differentiation by targeting the transcription factor c-myb. Cell 131: 146-159.