Construction and analysis of an integrated regulatory network derived from High-Throughput sequencing data

PLoS Computational Biology

Volumn 7, Issue 11, 2011, Pages

  Cheng, Chao ^a   Yan, Koon Kiu ^a   Hwang, Woochang ^b   Qian, Jiang ^b   Bhardwaj, Nitin ^a   Rozowsky, Joel ^a   Lu, Zhi John ^a   Niu, Wei ^c   Alves, Pedro ^a   Kato, Masaomi ^a   Snyder, Michael ^d   Gerstein, Mark ^a,e  

^a YALE UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e Yale University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DATA INTEGRATION; RNA; THROUGHPUT; TRANSCRIPTION;

BINDING PROFILES; CLASSIFIEDS; HIGH-THROUGHPUT; HIGH-THROUGHPUT SEQUENCING; MULTILEVELS; NEGATIVE REGULATORS; NETWORK FRAMEWORKS; REGULATORY NETWORK; SYSTEMATIC INTEGRATION; TARGET GENES;

TRANSCRIPTION FACTORS;

MICRORNA; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EMBEDDING; GENE CONTROL; GENE INTERACTION; GENE LOCATION; GENE REGULATORY NETWORK; GENE STRUCTURE; GENE TARGETING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC DATABASE; HIGH THROUGHPUT SEQUENCING; NONHUMAN; PROCESS DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY RNA SEQUENCE; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; CLUSTER ANALYSIS; DNA MICROARRAY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METHODOLOGY;

CAENORHABDITIS ELEGANS; EUKARYOTA;

ANIMALS; CAENORHABDITIS ELEGANS; CLUSTER ANALYSIS; DATABASES, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; MICRORNAS; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 81355164253     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002190     Document Type: Article

References (79)

1. Levine M, Tjian R, (2003) Transcription regulation and animal diversity. Nature 424: 147-151.
2. Moore MJ, (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309: 1514-1518.
3. Chen K, Rajewsky N, (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8: 93-103.
4. Wray GA, Hahn MW, Abouheif E, Balhoff JP, Pizer M, et al. (2003) The evolution of transcriptional regulation in eukaryotes. Mol Biol Evol 20: 1377-1419.
5. Ambros V, (2004) The functions of animal microRNAs. Nature 431: 350-355.
6. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
7. Hobert O, (2004) Common logic of transcription factor and microRNA action. Trends Biochem Sci 29: 462-468.
8. Brennecke J, Stark A, Russell RB, Cohen SM, (2005) Principles of microRNA-target recognition. PLoS Biol 3: e85.
9. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, et al. (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
10. Lall S, Grun D, Krek A, Chen K, Wang YL, et al. (2006) A genome-wide map of conserved microRNA targets in C. elegans. Curr Biol 16: 460-471.
11. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, et al. (2002) Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804.
12. Johnston RJ Jr, Chang S, Etchberger JF, Ortiz CO, Hobert O, (2005) MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci U S A 102: 12449-12454.
13. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, et al. (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123: 819-831.
14. Barabasi AL, Oltvai ZN, (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113.
15. Stites EC, Trampont PC, Ma Z, Ravichandran KS, (2007) Network analysis of oncogenic Ras activation in cancer. Science 318: 463-467.
16. Said MR, Begley TJ, Oppenheim AV, Lauffenburger DA, Samson LD, (2004) Global network analysis of phenotypic effects: protein networks and toxicity modulation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101: 18006-18011.
17. Bhardwaj N, Yan KK, Gerstein MB, (2010) Analysis of diverse regulatory networks in a hierarchical context shows consistent tendencies for collaboration in the middle levels. Proc Natl Acad Sci U S A 107: 6841-6846.
18. Yan KK, Fang G, Bhardwaj N, Alexander RP, Gerstein M, (2010) Comparing genomes to computer operating systems in terms of the topology and evolution of their regulatory control networks. Proc Natl Acad Sci U S A 107: 9186-9191.
19. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298: 824-827.
20. Shen-Orr SS, Milo R, Mangan S, Alon U, (2002) Network motifs in the transcriptional regulation network of Escherichia coli. Nat Genet 31: 64-68.
21. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
22. Conant GC, Wagner A, (2003) Convergent evolution of gene circuits. Nat Genet 34: 264-266.
23. Alon U, (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8: 450-461.
24. Yu X, Lin J, Zack DJ, Mendell JT, Qian J, (2008) Analysis of regulatory network topology reveals functionally distinct classes of microRNAs. Nucleic Acids Res 36: 6494-6503.
25. Shalgi R, Lieber D, Oren M, Pilpel Y, (2007) Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLoS Comput Biol 3: e131.
26. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, et al. (2008) A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev 22: 2535-2549.
27. Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927-930.
28. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775-1787.
29. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, et al. (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1797.
30. Johnson DS, Mortazavi A, Myers RM, Wold B, (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502.
31. Wang Z, Gerstein M, Snyder M, (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
32. Mangone M, Manoharan AP, Thierry-Mieg D, Thierry-Mieg J, Han T, et al. (2010) The landscape of C. elegans 3′UTRs. Science 329: 432-435.
33. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
34. Barski A, Jothi R, Cuddapah S, Cui K, Roh TY, et al. (2009) Chromatin poises miRNA- and protein-coding genes for expression. Genome Res 19: 1742-1751.
35. Cheng C, Yan KK, Yip KY, Rozowsky J, Alexander R, et al. (2011) A statistical framework for modeling gene expression using chromatin features and application to modENCODE datasets. Genome Biol 12: R15.
36. Johnson SM, Lin SY, Slack FJ, (2003) The time of appearance of the C. elegans let-7 microRNA is transcriptionally controlled utilizing a temporal regulatory element in its promoter. Dev Biol 259: 364-379.
37. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, et al. (2005) RAS is regulated by the let-7 microRNA family. Cell 120: 635-647.
38. Li M, Jones-Rhoades MW, Lau NC, Bartel DP, Rougvie AE, (2005) Regulatory mutations of mir-48, a C. elegans let-7 family MicroRNA, cause developmental timing defects. Dev Cell 9: 415-422.
39. Yoo AS, Greenwald I, (2005) LIN-12/Notch activation leads to microRNA-mediated down-regulation of Vav in C. elegans. Science 310: 1330-1333.
40. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ, (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158.
41. Chen X, Xu H, Yuan P, Fang F, Huss M, et al. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
42. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775-1787.
43. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
44. Friedman RC, Farh KK, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
45. Bhardwaj N, Carson MB, Abyzov A, Yan KK, Lu H, et al. (2010) Analysis of combinatorial regulation: scaling of partnerships between regulators with the number of governed targets. PLoS Comput Biol 6: e1000755.
46. Wang W, Cherry JM, Nochomovitz Y, Jolly E, Botstein D, et al. (2005) Inference of combinatorial regulation in yeast transcriptional networks: a case study of sporulation. Proc Natl Acad Sci U S A 102: 1998-2003.
47. Warmflash A, Dinner AR, (2008) Signatures of combinatorial regulation in intrinsic biological noise. Proc Natl Acad Sci U S A 105: 17262-17267.
48. Ravasi T, Suzuki H, Cannistraci CV, Katayama S, Bajic VB, et al. (2010) An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140: 744-752.
49. Yu X, Lin J, Zack DJ, Qian J, (2006) Computational analysis of tissue-specific combinatorial gene regulation: predicting interaction between transcription factors in human tissues. Nucleic Acids Res 34: 4925-4936.
50. Zhou Y, Ferguson J, Chang JT, Kluger Y, (2007) Inter- and intra-combinatorial regulation by transcription factors and microRNAs. BMC Genomics 8: 396.
51. Tsang J, Zhu J, van Oudenaarden A, (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753-767.
52. Moerman DG, Barstead RJ, (2008) Towards a mutation in every gene in Caenorhabditis elegans. Brief Funct Genomic Proteomic 7: 195-204.
53. Yu H, Gerstein M, (2006) Genomic analysis of the hierarchical structure of regulatory networks. Proc Natl Acad Sci U S A 103: 14724-14731.
54. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
55. Smith SB, Watada H, Scheel DW, Mrejen C, German MS, (2000) Autoregulation and maturity onset diabetes of the young transcription factors control the human PAX4 promoter. J Biol Chem 275: 36910-36919.
56. Bai G, Sheng N, Xie Z, Bian W, Yokota Y, et al. (2007) Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev Cell 13: 283-297.
57. Packer AI, Crotty DA, Elwell VA, Wolgemuth DJ, (1998) Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125: 1991-1998.
58. Aota S, Nakajima N, Sakamoto R, Watanabe S, Ibaraki N, et al. (2003) Pax6 autoregulation mediated by direct interaction of Pax6 protein with the head surface ectoderm-specific enhancer of the mouse Pax6 gene. Dev Biol 257: 1-13.
59. Rosenfeld N, Elowitz MB, Alon U, (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323: 785-793.
60. Wernicke S, (2006) Efficient detection of network motifs. IEEE/ACM Trans Comput Biol Bioinform 3: 347-359.
61. Wernicke S, Rasche F, (2006) FANMOD: a tool for fast network motif detection. Bioinformatics 22: 1152-1153.
62. Mangan S, Alon U, (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci U S A 100: 11980-11985.
63. Mangan S, Zaslaver A, Alon U, (2003) The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J Mol Biol 334: 197-204.
64. Kalir S, Mangan S, Alon U, (2005) A coherent feed-forward loop with a SUM input function prolongs flagella expression in Escherichia coli. Mol Syst Biol 1: 2005 0006.
65. Braun P, Tasan M, Dreze M, Barrios-Rodiles M, Lemmens I, et al. (2009) An experimentally derived confidence score for binary protein-protein interactions. Nat Methods 6: 91-97.
66. Liang H, Li WH, (2007) MicroRNA regulation of human protein protein interaction network. RNA 13: 1402-1408.
67. Yu H, Xia Y, Trifonov V, Gerstein M, (2006) Design principles of molecular networks revealed by global comparisons and composite motifs. Genome Biol 7: R55.
68. Baskerville S, Bartel DP, (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11: 241-247.
69. Re A, Cora D, Taverna D, Caselle M, (2009) Genome-wide survey of microRNA-transcription factor feed-forward regulatory circuits in human. Mol Biosyst 5: 854-867.
70. Lewis H, (2005) International outbreak of Salmonella Goldcoast infection in tourists returning from Majorca, September-October 2005: final summary. Euro Surveill 10: E051208 051203.
71. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM, (2005) Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123: 1133-1146.
72. Rajewsky N, (2006) microRNA target predictions in animals. Nat Genet 38 (Suppl): S8-13.
73. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, et al. (2010) Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330: 1787-1797.
74. Rozowsky J, Euskirchen G, Auerbach RK, Zhang ZD, Gibson T, et al. (2009) PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 27: 66-75.
75. Zhong M, Niu W, Lu ZJ, Sarov M, Murray JI, et al. (2010) Genome-wide identification of binding sites defines distinct functions for Caenorhabditis elegans PHA-4/FOXA in development and environmental response. PLoS Genet 6: e1000848.
76. Hillier LW, Reinke V, Green P, Hirst M, Marra MA, et al. (2009) Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res 19: 657-666.
77. Kato M, de Lencastre A, Pincus Z, Slack FJ, (2009) Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 10: R54.
78. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, et al. (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 38: D463-467.
79. Maslov S, Sneppen K, (2005) Computational architecture of the yeast regulatory network. Phys Biol 2: S94-100.