The interplay between transcription factors and microRNAs in genome-scale regulatory networks

BioEssays

Volumn 31, Issue 4, 2009, Pages 435-445

  Martinez, Natalia J ^a   Walhout, Albertha J M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

MicroRNA; Network motif; Regulatory network; Transcription factor

Indexed keywords

MICRORNA; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ANIMAL BEHAVIOR; DEVELOPMENT; DNA SEQUENCE; FEEDBACK SYSTEM; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENOMICS; HOMEOSTASIS; NONHUMAN; PROTEIN PROTEIN INTERACTION; REGULATORY SEQUENCE; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; GENE REGULATORY NETWORKS; GENOME; HUMANS; MICRORNAS; TRANSCRIPTION FACTORS;

METAZOA;

EID: 65449151411     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200800212     Document Type: Review

References (104)

1. The C. elegans Sequencing Consortium, Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998. 282: 2012-2018.
2. Adams, M. D., et al. The genome sequence of Drosophila melanogaster. Science 2000. 287: 2185-2195.
3. Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 2002. 420: 520-562.
4. Maniatis, T. and Tasic, B., Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 2002. 418: 236-243.
5. Levine, M. and Tjian, R., Transcription regulation and animal diversity. Nature 2003. 424: 147-151.
6. Mattick, J. S., RNA regulation: a new genetics? Nat Rev Genet 2004. 5: 316-323.
7. Kummerfeld, S. K. and Teichmann, S. A., DBD: a transcription factor prediction database. Nucleic Acids Res 2006. 34: D74-D81.
8. Reece-Hoyes, J. S., Deplancke, B., Shingles, J., Grove, C. A., Hope, I. A., et al. A compendium of C. elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biol 2005. 6: R110.
9. Wilson, D., Charoensawan, V., Kummerfeld, S. K. and Teichmann, S. A., DBD taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Res 2008. 36: D88-D92.
10. Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B. J., Chiang, H. R., et al. Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 2008. 455: 1193-1197.
11. Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A. and Enright, A. J., miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006. 34: D140-D144.
12. Brennecke, J., Stark, A., Russell, R. B. and Cohen, S. M., Principles of microRNA-target recognition. PLoS Biol 2005. 3: e85.
13. Krek, A., Grun, D., Poy, M. N., Wolf, R., Rosenberg, L., et al. Combinatorial microRNA target predictions. Nat Genet 2005. 37: 495-500.
14. Lall, S., Grun, D., Krek, A., Chen, K., Wang, Y. L., et al. A Genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 2006. 16: 460-471.
15. Lewis, B. P., Burge, C. B. and Bartel, D. P., Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005. 120: 15-20.
16. Latchman, D. S., Eukaryotic transcription factors, San Diego, Academic Press. 1998.
17. Lee, T. I. and Young, R. A., Transcription of eukaryotic protein-coding genes. Annu Rev Genet 2000. 34: 77-137.
18. Noyes, M. B., Christensen, R. G., Wakabayashi, A., Stormo, G. D. and Brodsky, M. H., Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 2008. 133: 1277-1289.
19. Wolfe, S. A., Nekludova, L. and Pabo, C. O., DNA recognition by Cys2His2 zinc finger proteins. Annu Rev Biophys Biomol Struct 2000. 29: 183-212.
20. Hollenhorst, P. C., Shah, A. A., Hopkins, C. and Graves, B. J., Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev 2007. 21 1882-1894.
21. Ow, M. C., Martinez, N. J., Olsen, P., Silverman, S., Barrasa, M. I., et al. The FLYWCH transcription factors FLH-1, FLH-2 and FLH-3 repress embryonic expression of microRNA genes in C. elegans. Genes Dev 2008. 22: 2520-2534.
22. The ENCODE Project Consortium. Identification and analysis of functional elements in 1%of the human genome by the ENCODE pilot project. Nature 2007. 447: 799-816.
23. Deplancke, B., Mukhopadhyay, A., Ao, W., Elewa, A. M., Grove, C. A., et al. A gene-centered C. elegans protein-DNA interaction network. Cell 2006. 125: 1193-1205.
24. Martinez, N. J., Ow, M. C., Barrasa, M. I., Hammell, M., Sequerra, R., et al. A genome-scale microRNA regulatory network in C. elegans reveals composite feedback motifs that provide high information flow. Genes Dev 2008a. 22: 2535-2549.
25. Vermeirssen, V., Barrasa, M. I., Hidalgo, C., Babon, J. A. B., Sequerra, R., et al. Transcription factor modularity in a gene-centered C. elegans core neuronal protein-DNA interaction network. Genome Res 2007. 17: 1061-1071.
26. Hall, D. A., Zhu, H., Zhu, X., Royce, T., Gerstein, M., et al. Regulation of gene expression by a metabolic enzyme. Science 2004. 306: 482-484.
27. Kim, V. N. and Nam, J. W., Genomics of microRNA. Trends Genet 2006. 22: 165-173.
28. Berezikov, E., Guryev, V., van de Belt, J., Wienholds, E., Plasterk, R. H., et al. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005. 120: 21-24.
29. Lagos-Quintana, M., Rauhut, R., Lendeckel, W. and Tuschl, T., Identification of novel genes coding for small expressed RNAs. Science 2001. 294: 853-858.
30. Lai, E. C., Tomancak, P., Williams, R. W. and Rubin, G. M., Computational identification of Drosophila microRNA genes. Genome Biol 2003. 4: R42.
31. Lau, N. C., Lim, L. P., Weinstein, E. G. and Bartel, D. P., An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 2001. 294: 858-862.
32. Lee, R. C., Feinbaum, R. L. and Ambros, V., The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993. 75: 843-854.
33. Lim, L. P., Lau, N. C., Weinstein, E. G., Abdelhakim, A., Yekta, S., et al. The microRNAs of Caenorhabditis elegans. Genes Dev 2003. 17: 991-1008.
34. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007. 129: 1401-1414.
35. Ruby, J. G., Jan, C., Player, C., Axtell, M. J., Lee, W., et al. Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 2006. 127: 1193-1207.
36. Ruby, J. G., Stark, A., Johnston, W. K., Kellis, M., Bartel, D. P., et al. Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 2007. 17: 1850-1864.
37. Filipowicz, W., Bhattacharyya, S. N. and Sonenberg, N., Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008. 9: 102-114.
38. Hertel, J., Lindemeyer, M., Missal, K., Fried, C., Tanzer, A., et al. The expansion of the metazoan microRNA repertoire. BMC Genomics 2006. 15. 25.
39. Abbott, A. L., Alvarez-Saavedra, E., Miska, E. A., Lau, N. C., Bartel, D. P., et al. The let-7 microRNA family members mir-48, mir-84 and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev Cell 2005. 9: 403-414.
40. Miska, E. A., Alvarez-Saavedra, E., Abbott, A. L., Lau, N. C., Hellman, A. B., et al. Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 2007. 3: e215.
41. Bryne, J. C., Valen, E., Tang, M. H., Marstrand, T., Winther, O., et al. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res 2008. 36: D102-D106.
42. Wingender, E., Chen, X., Fricke, E., Geffers, R., Hehl, R., et al. The TRANSFAC system on gene expression regulation. Nucleic Acids Res 2001. 29: 281-283.
43. Berger, M. F., Badis, G., Gehrke, A. R., Talukder, S., Philippakis, A. A., et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008. 133: 1266-1276.
44. Rajewski, N., microRNA target prediction in animals. Nat Genet 2006. 38: S8-S13.
45. Mazumder, B., Seshadri, V. and Fox, P. L., Translational control by the 3′ UTR: the ends specify the means. Trends Biochem Sci 2003. 28: 91-98.
46. Retelska, D., Iseli, C., Bucher, P., Jongeneel, C. V. and Naef, F., Similarities and differences of polyadenylation signals in human and fly. BMC Genomics 2006. 12: 176.
47. Lytle, J. R., Yario, T. A. and Steitz, J. A., Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5′ UTR as in the 3′ UTR. Proc Natl Acad Sci USA 2007. 104: 9667-9672.
48. Duursma, A. M., Kedde, M., Schrier, M., le Sage, C. and Agami, R., miR-148 targets human DNMT3b protein coding region. RNA 2008. 14: 872-877.
49. Tay, Y., Zhang, J., Thomson, A. M., Lim, B. and Rigoutsos, I., MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008. 455: 1124-1128.
50. Chang, S., Johnston, R. J., Jr., Frokjaer-Jensen, C., Lockery, S. and Hobert, O., MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 2004. 430: 785-789.
51. Johnson, S. M., Lin, S. Y. and Slack, F. J., The time of appearance of the C. elegans let-7 microRNA is transcriptionally controlled utilizing a temporal regulatory element in its promoter. Dev Biol 2003. 259: 364-379.
52. Martinez, N. J., Ow, M. C., Reece-Hoyes, J., Barrasa, M. I., Ambros, V., et al. Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. Genome Res 2008b. 18: 2005-2015.
53. Reece-Hoyes, J. S., Shingles, J., Dupuy, D., Grove, C. A., Walhout, A. J., et al. Insight into transcription factor gene duplication from Caenorhabditis elegans Promoterome-driven expression patterns. BMC Genomics 2007. 8: 27.
54. Obernosterer, G., Leuschner, P. J., Alenius, M. and Martinez, J., Post-transcriptional regulation of microRNA expression. RNA 2006. 12: 1161-1167.
55. Viswanathan, S. R., Daley, G. Q. and Gregory, R. I., Selective blockade of microRNA processing by Lin28. Science 2008. 320: 97-100.
56. Kedde, M., Strasser, M. J., Boldajipour, B., Oude Vrielink, J. A., Slanchev, K., et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 2007. 131: 1273-1286.
57. Grove, C. A. and Walhout, A. J., Transcription factor functionality and transcription regulatory networks. Molecular BioSystems 2008. 4: 309-314.
58. O'Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V. and Mendell, J. T., c-Myc-regulated microRNAs modulate E2F1 expression. Nature 2005. 435: 839-843.
59. Thomson, J. M., Newman, M., Parker, J. S., Morin-Kensicki, E. M., Wright, T., et al. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 2006. 20: 2202-2207.
60. Wulczyn, F. G., Smirnova, L., Rybak, A., Brandt, C., Kwidzinski, E., et al. Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J 2007. 21: 415-426.
61. Kawahara, Y., Zinshteyn, B., Sethupathy, P., Lizasa, H., Hatzigergiou, A. G., et al. Redirection of silencing targets by adenosine-toinosine editing of miRNAs. Science 2007. 315: 1137-1140.
62. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003. 421: 231-237.
63. Boutros, M., Kiger, A. A., Armknecht, S., Kerr, K., Hild, M., et al. Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 2004. 303: 832-835.
64. Mango, S. E., Lambie, E. J. and Kimble, J., The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development 1994. 120: 3019-3031.
65. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000. 403: 901-906.
66. Johnston, R. J. and Hobert, O., A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 2003. 426: 845-849.
67. Simon, D. J., Madison, J. M., Conery, A. L., Thompson-Peer, K. L., Soskis, M., et al. The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions. Cell 2008. 133: 891-902.
68. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., et al. Dicer is essential for mouse development. Nat Genet 2003. 35: 215-217.
69. Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E. and Tabin, C. J., The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci USA 2005. 102: 10898-10903.
70. Harris, K. S., Zhang, Z., McManus, M. T., Harfe, B. D. and Sun, X., Dicer function is essential for lung epithelium morphogenesis. Proc Natl Acad Sci USA 2006. 103: 2208-2213.
71. Cobb, B. S., Nesterova, T. B., Thompson, E., Hertweck, A., O'Connor, E., et al. T cell lineage choice and differentiation in the absence of the RNaseIII enzyme Dicer. J Exp Med 2005. 201: 1367-1373.
72. Giraldez, A. J., Cinalli, R. M., Glasner, M. E., Enright, A. J., Thomson, J. M., et al. MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005. 308: 833-838.
73. Muljo, S. A., Ansel, K. M., Kanellopoulou, C., Livingston, D. M., Rao, A., et al. Aberrant T cell differentiation in the absence of Dicer. J Exp Med 2005. 202: 261-269.
74. Wienholds, E., Koudijs, M. J., van Eeden, F. J., Cuppen, E. and Plasterk, R. H., The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat Genet 2003. 35: 217-218.
75. Hornstein, E. and Shomron, N., Canalization of development by microRNAs. Nat Genet 2006. 38: S20-24.
76. Jeong, H., Mason, S. P., Barabasi, A. L. and Oltvai, Z. N., Lethality and centrality in protein networks. Nature 2001. 411: 41-42.
77. Jeong, H., Tombor, B., Albert, R.,Oltvai, Z. N. and Barabasi, A. L., The large-scale organization of metabolic networks. Nature 2000. 407: 651-654.
78. Babu, M. M., Luscombe, N. M., Aravind, L., Gerstein, M. and Teichmann, S. A., Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol 2004. 14: 283-291.
79. Shalgi, R., Lieber, D., Oren, M. and Pilpel, Y., Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLoS Comput Biol 2007. 3: e131.
80. Bartel, D. P. and Chen, C. Z., Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 2004. 5: 396-400.
81. Barabasi, A. L. and Oltvai, Z. N., Network biology: understanding the cell's functional organization. Nat Rev Genet 2004. 5: 101-113.
82. Milo, R., Shen-Orr, S., Itzkovitz, S., Kashtan, N., Chklovskii, D., et al. Network motifs: simple building blocks of complex networks. Science 2002. 298: 824-827.
83. Shen-Orr, S. S., Milo, R., Mangan, S. and Alon, U., Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 2002. 31: 64-68.
84. Yeger-Lotem, E., Sattath, S., Kashtan, N., Itzkovitz, S., Milo, R., et al. Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. Proc Natl Acad Sci USA 2004. 101: 5934-5939.
85. Tsang, J., Zhu, J. and van Oudenaarden, A., MicroRNA-mediated feedback and feed forward looops are recurrent network motifs in mammals. Mol Cell 2007. 26: 753-767.
86. Fazi, F., Rosa, A., Fatica, A., Gelmetti, V., De Marchis, M. L., et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBP alpha regulates human granulopoiesis. Cell 2005. 123: 819-831.
87. Johnston, R. J., Chang, S., Etchberge, J. F., Ortiz, C. O. and Hobert, O., MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci USA 2005. 102: 12449-12454.
88. Kim, J., Inoue, K., Ishii, J., Vanti, W. B., Voronov, S. V., et al. A microRNA feedback circuit in midbrain dopamine neurons. Science 2007. 317: 1220-1224
89. Varghese, J. and Cohen, S. M., microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev 2007. 21: 2277-2282.
90. Becksei, A. and Serrano, L., Engineering stability in gene networks by autoregulation. Nature 2000. 405: 590-593.
91. Elowitz, M. B. and Leibler, S., A synthetic oscillatory network of transcriptional regulators. Nature 2000. 403: 335-338.
92. Gardner, T. S., Cantor, C. R. and Collins, J. J., Construction of a genetic toggle switch in Escherichia coli. Nature 2000. 403: 339-342.
93. Mangan, S. and Alon, U., Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA 2003. 100: 1985.
94. Hirata, H., Yoshiura, S., Ohtsuka, T., Bessho, Y., Harada, T., et al. Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 2002. 298: 840-843.
95. Alon, U., Network motifs: theory and experimental approaches. Nat Rev Genet 2007. 8: 450-461.
96. Sylvestre, Y., De Guire, V., Querido, E., Mukhopadhyay, U. K., Bourdeau, V., et al. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 2007. 282: 2135-2143.
97. Woods, K., Thomson, J. M. and Hammond, S. M., Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 2007. 282: 2130-2134.
98. Marson, A., Levine, S. S., Cole, M. F., Frampton, G. M., Brambrink, T., et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008. 134: 521-533.
99. Farh, K. K., Grimson, A., Jan, C., Lewis, B. P., Johnston, W. K., et al. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 2005. 310: 1817-1821.
100. Sood, P., Krek, A., Zavolan, M., Macino, G. and Rajewsky, N., Celltype- specific signatures of microRNAs on target mRNA expression. Proc Natl Acad Sci USA 2006. 103: 2746-2751.
101. Stark, A., Brennecke, J., Bushati, N., Russell, R. B. and Cohen, S. M., Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 2005. 123: 1133-1146.
102. Wang, X., Gu, J., Zhang, M. Q. and Li, Y., Identification of phylogenetically conserved microRNA cis-regulatory elements across 12 Drosophila species. Bioinformatics 2008. 24: 165-171.
103. Cui, Q., Yu, Z., Pan, Y., Purisima, E. O. and Wang, E., MicroRNAs preferentially target the genes with high transcriptional regulation complexity. BBRC 2007. 352: 733-738.
104. Liang, H. and Li, W. H., MicroRNA regulation of human protein-protein interaction network. RNA 2007. 13: 1402-1408.