MicroRNA-Mediated Feedback and Feedforward Loops Are Recurrent Network Motifs in Mammals

Molecular Cell

Volumn 26, Issue 5, 2007, Pages 753-767

  Tsang, John ^a,b   Zhu, Jun ^c,d   van Oudenaarden, Alexander ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c DUKE UNIVERSITY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

RNA; SYSBIO

Indexed keywords

MICRORNA;

ARTICLE; AUTOREGULATION; FEEDBACK SYSTEM; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; GENOME; HOMEOSTASIS; HUMAN; MATHEMATICAL ANALYSIS; MOUSE; NERVE CELL NETWORK; NONHUMAN; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; FEEDBACK; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICE; MICRORNAS; MODELS, GENETIC; NERVE NET; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

ANIMALIA; MAMMALIA;

EID: 34249819336     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.05.018     Document Type: Article

References (68)

1. Aboobaker A.A., Tomancak P., Patel N., Rubin G.M., and Lai E.C. Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc. Natl. Acad. Sci. USA 102 (2005) 18017-18022
2. Acar M., Becskei A., and van Oudenaarden A. Enhancement of cellular memory by reducing stochastic transitions. Nature 435 (2005) 228-232
3. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., and Macklis J.D. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45 (2005) 207-221
4. Ballas N., Grunseich C., Lu D.D., Speh J.C., and Mandel G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121 (2005) 645-657
5. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2004) 281-297
6. Bartel D.P., and Chen C.Z. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5 (2004) 396-400
7. Baskerville S., and Bartel D.P. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11 (2005) 241-247
8. Becskei A., and Serrano L. Engineering stability in gene networks by autoregulation. Nature 405 (2000) 590-593
9. Blake W.J., Balazsi G., Kohanski M.A., Isaacs F.J., Murphy K.F., Kuang Y., Cantor C.R., Walt D.R., and Collins J.J. Phenotypic consequences of promoter-mediated transcriptional noise. Mol. Cell 24 (2006) 853-865
10. Brandman O., Ferrell Jr. J.E., Li R., and Meyer T. Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 310 (2005) 496-498
11. Brennecke J., Stark A., Russell R.B., and Cohen S.M. Principles of microRNA-target recognition. PLoS Biol. 3 (2005) e85 10.1371/journal.pbio.0030085
12. Cao X., Yeo G., Muotri A.R., Kuwabara T., and Gage F.H. Noncoding RNAs in the mammalian central nervous system. Annu. Rev. Neurosci. 29 (2006) 77-103
13. Carthew R.W. Gene regulation by microRNAs. Curr. Opin. Genet. Dev. 16 (2006) 203-208
14. Chong J.A., Tapia-Ramirez J., Kim S., Toledo-Aral J.J., Zheng Y., Boutros M.C., Altshuller Y.M., Frohman M.A., Kraner S.D., and Mandel G. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80 (1995) 949-957
15. Conaco C., Otto S., Han J.J., and Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. USA 103 (2006) 2422-2427
16. Doench J.G., and Sharp P.A. Specificity of microRNA target selection in translational repression. Genes Dev. 18 (2004) 504-511
17. Doench J.G., Petersen C.P., and Sharp P.A. siRNAs can function as miRNAs. Genes Dev. 17 (2003) 438-442
18. Dostie J., Mourelatos Z., Yang M., Sharma A., and Dreyfuss G. Numerous microRNPs in neuronal cells containing novel microRNAs. RNA 9 (2003) 180-186
19. Eisen M.B., Spellman P.T., Brown P.O., and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95 (1998) 14863-14868
20. Enright A.J., John B., Gaul U., Tuschl T., Sander C., and Marks D.S. MicroRNA targets in Drosophila. Genome Biol. 5 (2003) R1 10.1186/gb-2003-5-1-r1
21. Esquela-Kerscher A., and Slack F.J. Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer 6 (2006) 259-269
22. Farh K.K., Grimson A., Jan C., Lewis B.P., Johnston W.K., Lim L.P., Burge C.B., and Bartel D.P. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310 (2005) 1817-1821
23. Fazi F., Rosa A., Fatica A., Gelmetti V., De Marchis M.L., Nervi C., and Bozzoni I. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123 (2005) 819-831
24. Ferrell Jr. J.E. Building a cellular switch: more lessons from a good egg. Bioessays 21 (1999) 866-870
25. Ferrell Jr. J.E. Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr. Opin. Cell Biol. 14 (2002) 140-148
26. Golding I., Paulsson J., Zawilski S.M., and Cox E.C. Real-time kinetics of gene activity in individual bacteria. Cell 123 (2005) 1025-1036
27. 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. 34 (2006) D140-D144
28. Hornstein E., and Shomron N. Canalization of development by microRNAs. Nat. Genet. 38 Suppl 1 (2006) S20-S24
29. Howard M.L., and Davidson E.H. cis-Regulatory control circuits in development. Dev. Biol. 271 (2004) 109-118
30. John B., Enright A.J., Aravin A., Tuschl T., Sander C., and Marks D.S. Human microRNA targets. PLoS Biol. 2 (2004) e363 10.1371/journal.pbio.0020363
31. Johnston Jr. R.J., Chang S., Etchberger 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 102 (2005) 12449-12454
32. Kaern M., Elston T.C., Blake W.J., and Collins J.J. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6 (2005) 451-464
33. Kiebler M.A., and Bassell G.J. Neuronal RNA granules: movers and makers. Neuron 51 (2006) 685-690
34. Kim Y.K., and Kim V.N. Processing of intronic microRNAs. EMBO J. 26 (2007) 775-783
35. Kim J., Krichevsky A., Grad Y., Hayes G.D., Kosik K.S., Church G.M., and Ruvkun G. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc. Natl. Acad. Sci. USA 101 (2004) 360-365
36. Kloosterman W.P., and Plasterk R.H. The diverse functions of microRNAs in animal development and disease. Dev. Cell 11 (2006) 441-450
37. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., and Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 37 (2005) 495-500
38. Lagos-Quintana M., Rauhut R., Yalcin A., Meyer J., Lendeckel W., and Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12 (2002) 735-739
39. 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 120 (2005) 15-20
40. Li X., and Carthew R.W. A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123 (2005) 1267-1277
41. Li Y., Wang F., Lee J.A., and Gao F.B. MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev. 20 (2006) 2793-2805
42. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., and Alon U. Network motifs: simple building blocks of complex networks. Science 298 (2002) 824-827
43. Miska E.A., Alvarez-Saavedra E., Townsend M., Yoshii A., Sestan N., Rakic P., Constantine-Paton M., and Horvitz H.R. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 5 (2004) R68 10.1186/gb-2004-5-9-r68
44. Mortazavi A., Thompson E.C., Garcia S.T., Myers R.M., and Wold B. Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. Genome Res. 16 (2006) 1208-1221
45. Obernosterer G., Leuschner P.J., Alenius M., and Martinez J. Post-transcriptional regulation of microRNA expression. RNA 12 (2006) 1161-1167
46. 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 435 (2005) 839-843
47. Pedraza J.M., and van Oudenaarden A. Noise propagation in gene networks. Science 307 (2005) 1965-1969
48. Raj A., Peskin C.S., Tranchina D., Vargas D.Y., and Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 4 (2006) e309 10.1371/journal.pbio.0040309
49. Rajewsky N. microRNA target predictions in animals. Nat. Genet. 38 Suppl (2006) S8-S13
50. Reich M., Liefeld T., Gould J., Lerner J., Tamayo P., and Mesirov J.P. GenePattern 2.0. Nat. Genet. 38 (2006) 500-501
51. Rodriguez A., Griffiths-Jones S., Ashurst J.L., and Bradley A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 14 (2004) 1902-1910
52. Rosenfeld N., Elowitz M.B., and Alon U. Negative autoregulation speeds the response times of transcription networks. J. Mol. Biol. 323 (2002) 785-793
53. Rosenfeld N., Young J.W., Alon U., Swain P.S., and Elowitz M.B. Gene regulation at the single-cell level. Science 307 (2005) 1962-1965
54. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., and Greenberg M.E. A brain-specific microRNA regulates dendritic spine development. Nature 439 (2006) 283-289
55. Sempere L.F., Freemantle S., Pitha-Rowe I., Moss E., Dmitrovsky E., and Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5 (2004) R13
56. Shen-Orr S.S., Milo R., Mangan S., and Alon U. Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 31 (2002) 64-68
57. Sood P., Krek A., Zavolan M., Macino G., and Rajewsky N. Cell-type-specific signatures of microRNAs on target mRNA expression. Proc. Natl. Acad. Sci. USA 103 (2006) 2746-2751
58. 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 123 (2005) 1133-1146
59. Su A.I., Wiltshire T., Batalov S., Lapp H., Ching K.A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 101 (2004) 6062-6067
60. Sugino K., Hempel C.M., Miller M.N., Hattox A.M., Shapiro P., Wu C., Huang Z.J., and Nelson S.B. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9 (2006) 99-107
61. Sylvestre Y., De Guire V., Querido E., Mukhopadhyay U.K., Bourdeau V., Major F., Ferbeyre G., and Chartrand P. An E2F/miR-20a auto-regulatory feed-back loop. J. Biol. Chem. 282 (2006) 2135-2143
62. Thomson J.M., Newman M., Parker J.S., Morin-Kensicki E.M., Wright T., and Hammond S.M. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 20 (2006) 2202-2207
63. Valencia-Sanchez M.A., Liu J., Hannon G.J., and Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20 (2006) 515-524
64. Wheeler D.L., Barrett T., Benson D.A., Bryant S.H., Canese K., Chetvernin V., Church D.M., DiCuccio M., Edgar R., Federhen S., et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 34 (2006) D173-D180
65. Wu J., and Xie X. Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol. 7 (2006) R85
66. Wulczyn F.G., Smirnova L., Rybak A., Brandt C., Kwidzinski E., Ninnemann O., Strehle M., Seiler A., Schumacher S., and Nitsch R. Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J. 21 (2007) 415-426
67. Xie X., Lu J., Kulbokas E.J., Golub T.R., Mootha V., Lindblad-Toh K., Lander E.S., and Kellis M. Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature 434 (2005) 338-345
68. Yoo A.S., and Greenwald I. LIN-12/Notch activation leads to microRNA-mediated down-regulation of Vav in C. elegans. Science 310 (2005) 1330-1333