Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics

PLoS Computational Biology

Volumn 4, Issue 3, 2008, Pages

  Ramsey, Stephen A ^a   Klemm, Sandy L ^a   Zak, Daniel E ^a   Kennedy, Kathleen A ^a   Thorsson, Vesteinn ^a   Li, Bin ^a   Gilchrist, Mark ^a   Gold, Elizabeth S ^a   Johnson, Carrie D ^a   Litvak, Vladimir ^a   Navarro, Garnet ^a   Roach, Jared C ^a   Rosenberger, Carrie M ^a   Rust, Alistair G ^a   Yudkovsky, Natalya ^a   Aderem, Alan ^a   Shmulevich, Ilya ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; CHEMICAL ACTIVATION; MAMMALS; TRANSCRIPTION; TRANSCRIPTION FACTORS;

DATATYPES; EXPRESSION DYNAMICS; IMMUNE CELLS; MACROPHAGE ACTIVATION; MURINE MACROPHAGES; PATHOGEN-ASSOCIATED MOLECULAR PATTERNS; TOLL-LIKE RECEPTORS; TRANSCRIPTIONAL NETWORKS; TRANSCRIPTIONAL PROGRAM; TRANSCRIPTIONAL REGULATORY NETWORKS;

MACROPHAGES;

TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA SEQUENCE; GENE; GENE CLUSTER; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; TRANSCRIPTION FACTOR GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; KINETICS; METABOLISM; PHYSIOLOGY; PROTEIN MOTIF; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; SYSTEM ANALYSIS; TRANSACTIVATION;

MAMMALIA; MURINAE;

AMINO ACID MOTIFS; ANIMALS; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; HUMANS; KINETICS; MACROPHAGE ACTIVATION; MACROPHAGES; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; SYSTEMS INTEGRATION; TOLL-LIKE RECEPTORS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

EID: 41849123062     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000021     Document Type: Article

References (96)

1. Underhill DM, Ozinsky A (2002) Toll-like receptors: key mediators of microbe detection. Curr Opin Immunol 14: 103-110.
2. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21: 335-376.
3. Hoebe K, Du X, Georgel P, Janssen E, Tabeta K, et al. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424: 743-748.
4. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, et al. (2003) Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301: 640-643.
5. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1 and IL-18-mediated function. Immunity 9: 143-150.
6. Gilchrist M, Thorsson V, Li B, Rust AG, Korb M, et al. (2006) Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441: 173-178.
7. Nilsson R, Bajic VB, Suzuki H, di Bernardo D, Björkegren J, et al. (2006) Transcriptional network dynamics in macrophage activation. Genomics 88: 133-142.
8. Nau GJ, Richmond JFL, Schlesinger A, Jennings EG, Lander ES, et al. (2002) Human macrophage activation programs induced by bacterial pathogens. Proc Natl Acad Sci USA 99: 1503-1508.
9. Jenner RG, Young RA (2005) Insights into host responses against pathogens from transcriptional profiling. Nature Rev Microbiol 3: 281-294.
10. Sasmono RT, Hume DA (2004) The biology of macrophages. In: Kauffmann SHE, ed (2004) The innate immune response to infection. Washington, DC: American Society for Microbiology.
11. Basso K, Margolin AA, Stolovitzky G, Klein U, Dalla-Favera R, et al. (2005) Reverse engineering of regulatory networks in human B cells. Nat Gen 37: 382-390.
12. Bonneau R, Reiss DJ, Shannon P, Facciotti M, Hood L, et al. (2006) The Inferelator: an algorithm for learning parsimonious regulatory networks from systems biology data sets de novo. Genome Biol 7: R36.
13. Haverty PM, Hansen U, Weng Z (2004) Computational inference of transcriptional regulatory networks from expression profiling and transcription factor binding site identification. Nucleic Acids Res 32: 179-188.
14. Wang Y, Joshi T, Zhang XS, Xu D, Chen L (2006) Inferring gene regulatory networks from multiple microarray datasets. Bioinformatics 22: 2413-2120.
15. Zhao W, Serpedin E, Dougherty ER (2006) Inferring gene regulatory networks from time series data using the minimum description length principle. Bioinformatics 22: 2129-2135.
16. VanBuren V, Ko MSH (2004) Regulation of genome activity and genetic networks. In: Ruvinsky A, Marshall Graves JA, eds (2004) Mammalian Genomics. Oxfordshire, U.K.: CABI Publishing.
17. Honda K, Taniguchi T (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nature Rev Immunol 6: 644-659.
18. Chiang DY, Brown PO, Eisen MB (2001) Visualizing associations between genome sequences and gene expression data using genome-mean expression profiles. Bioinformatics 17: S49-S55.
19. Holloway DT, Kon M, DeLisi C (2005) Integrating genomic data to predict transcription factor binding. Genome Inform 16: 83-94.
20. Elkon R, Linhart C, Sharan R, Shamir R, Shiloh Y (2003) Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res 13: 773-780.
21. Zou M, Conzen SD (2005) A new dynamic Bayesian network (DBN) approach for identifying gene regulatory networks from time course microarray data. Bioinformatics 21: 71-79.
22. Arkin A, Shen P, Ross J (1997) A test case of correlation metric construction of a reaction pathway from measurements. Science 277: 1275-1279.
23. Agrawal A, Mittal A (2005) A dynamic time-lagged correlation based method to learn multi-time delay gene networks. Enformatika 9: 167-174.
24. Chen T, VFilkov V, Skiena SS (2001) Identifying gene regulatory networks from experimental data. Parallel Comput 27: 141-162.
25. Kato M, Tsunoda T, Takagi T (2001) Lag analysis of genetic networks in the cell cycle of budding yeast. In: Matsuda H, Miyano S, Takagi T, Wong L, eds (2001) Genome Informatics 2001; Tokyo. Tokyo: Universal Academy Press.
26. Schmitt WAJ, Raab RM, Stephanopoulos G (2004) Elucidation of gene interaction networks through time-lagged correlation analysis of transcriptional data. Genome Res 14: 1654-1663.
27. Shaw OJ, Harwood C, Steggles LJ, Wipat A (2004) SARGE: a tool for creation of putative genetic networks. Bioinformatics 20: 3638-3640.
28. Wu W-S, Li W-H, Chen B-S (2006) Computational reconstruction of transcriptional regulatory modules of the yeast cell cycle. BMC Bioinform 7: 421.
29. Raab RM (2006) Incorporating genome-scale tools for studying energy homeostasis. Nutr Metab (Lond) 3: 40.
30. Hartman MG, Lu D, Kim ML, Kociba GJ, Shukri T, et al. (2004) Role for activating transcription factor 3 in stress-induced beta-cell apoptosis. Mol Cell Biol 24: 5721-5732.
31. Blendy JA, Kaestner KH, Weinbauer GF, Neischlag E, Schütz G (1996) Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380: 162-165.
32. Storey JD, Xiao W, Leek JT, Tompkins RG, Davis RW (2005) Significance analysis of time course microarray experiments. Proc Natl Acad Sci U S A 102: 12837-12842.
33. Wingender E, Dietze P, Karas H, Knuppel R (1996) TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res 24: 238-241.
34. Hayden MS, West AP, Ghosh S (2006) NFκB and the immune response. Oncogene 25: 6758-6780.
35. Foletta VC, Segal DH, Cohen DR (1998) Transcriptional regulation in the immune system: all roads lead to AP-1. J Leukoc Biol 63: 139-152.
36. Ivashkiv LB (2000) Jak-STAT signaling pathways in cells of the immune system. Rev Immunogenet 2: 220-230.
37. Stanton LW, Garrard LJ, Damm D, Garrick BL, Lam A, et al. (2000) Altered patterns of gene expression in response to myocardial infarction. Circulation Res 86: 939-945.
38. Hastie T, Tibshirani R, Friedman JH (2003) The elements of statistical learning. New York: Springer.
39. Barrio M, Burrage K, Leier A, Tian T (2006) Oscillatory regulation of Hes1: discrete stochastic delay modelling and simulation. PLoS Comp Biol 2: 1017-1030.
40. LeMaire MF, Thummel CS (1990) Splicing precedes polyadenylation during Drosophila E74A transcription. Mol Cell Biol 10: 6059-6063.
41. Monk NAM (2003) Oscillatory expression of Hes1, p53, and NK-κB driven by transcriptional time delays. Curr Biol 13: 1409-1413.
42. Zak DE (2005) Structured modeling of mammalian transcription networks. NewarkDE: University of Delaware. pp 374.
43. Cogswell PC, Scheinman RI, Baldwin AS Jr (1993) Promoter of the human NF-kappa B p50/p105 gene. Regulation by NF-kappa B subunits and by c-REL. J Immunol 150: 2794-2804.
44. Barnes BJ, Richards J, Mancl M, Hanash S, Beretta L, et al. (2004) Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J Biol Chem 279: 45194-45207.
45. Yu J, Xiao J, Ren X, Lao K, Xie S (2006) Probing gene expression in live cells, one protein molecule at a time. Science 311: 1600-1603.
46. Arkin A, Ross J (1995) Statistical construction of chemical-reaction mechanisms from measured time-series. J Phys Chem 99: 970-979.
47. Kuhn RM, Karolchik D, Zweig AS, Trumbower H, Thomas DJ, et al. (2007) The UCSC genome browser database: update 2007. Nucleic Acids Res 35: D668-D673.
48. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, et al. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32: 1372-1381.
49. Rahman A, Anwar KN, True AL, Malik AB (1999) Thrombin-induced p65 homodimer binding to downstream NF-kappa B site of the promoter mediates endothelial ICAM-1 expression and neutrophil adhesion. J Immunol 162: 5466-5476.
50. Hu HM, Tian Q, Baer M, Spooner CJ, Williams SC, et al. (2000) The C/EBP bZIP domain can mediate lipopolysaccharide induction of the proinflammatory cytokines interleukin-6 and monocyte chemoattractant protein-1. J Biol Chem 275: 16373-16381.
51. Hwang D, Rust AG, Ramsey S, Smith JJ, Leslie DM, et al. (2005) A data integration methodology for systems biology. Proc Nat Acad Sci U S A 102: 17296-17301.
52. Barabasi AL, Oltvai ZN (2004) Network biology: understanding the cell's functional organization. Nat Rev Genet 5: 101-113.
53. Mukherjee B, Morgenbesser SD, DePinho RA (1992) Myc family oncoproteins function through a common pathway to transform normal cells in culture: cross-interference by Max and trans-activating dominant mutants. Genes Dev 6: 1480-1492.
54. Attwooll C, Lazzerini DE, Helin K (2004) The E2F family: specific functions and overlapping interests. EMBO J 23: 4709-4716.
55. Chen F, Ogawa K, Liu X, Stringfield TM, Chen Y (2002) Repression of Smad2 and Smad3 transactivating activity by association with a novel splice variant of CCAAT-binding factor C subunit. Biochem J 364: 571-577.
56. Marziali G, Perrotti E, Ilari R, Coccia EM, Mantovani R, et al. (1999) The ativity of CCAAT-box binding factor NF-Y is modulated through the regulated expression of its A subunit during monocyte to macrophage differentiation: regulation of tissue-specific genes through a ubiquitous transcription factor. Blood 93: 519-526.
57. Castrillo A, Tontonoz P (2004) Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation. Annu Rev Cell Dev Biol 20: 455-480.
58. Shakhov AN, Collart MA, Vassalli P, Nedospasov SA, Jongeneel CV (1990) Kappa B-type enhancers are involved in lipopolysaccharide-mediated transcriptional activation of the tumor necrosis factor alpha gene in primary macrophages. J Exp Med 171: 35-47.
59. Kim HS, Lee M-S (2007) STAT1 as a key modulator of cell death. Cell Signal 19: 454-465.
60. Potapov AP, Voss N, Sasse N, Wingender E (2005) Topology of mammalian transcription networks. Genome Inform 16: 270-278.
61. Chastel C, Jiricny J, Jaussi R (2004) Activation of stress-responsive promoters by ionizing radiation for deployment in targeted gene therapy. DNA Repair 3: 201-215.
62. Liu J, Guan X, Ma X (2005) Interferon regulatory factor 1 is an essential and direct transcriptional activator for IFNg-induced RANTES/CCL5 expression in macrophages. J Biol Chem 280: 24347-24355.
63. Mostecki J, Showalter BM, Rothman PB (2005) Early growth response-1 regulates lipopolysaccharide-induced suppressor of cytokine signaling-1 transcription. J Biol Chem 280: 2596-2605.
64. Hirano S, Anuradha CD, Kanno S (2000) Transcription of krox-20/egr-2 is upregulated after exposure to fibrous particles and adhesion in rat alveolar macrophages. Am J Resipir Cell Mol Biol 23: 313-319.
65. Chavrier P, Zerial M, Lemaire P, Almendral J, Bravo R, et al. (1988) A gene encoding a protein with zinc fingers is activated during G0/G1 transition in cultured cells. EMBO J 7: 29-35.
66. Carey B, Sataudt MK, Bonaminio D, van der Loo JC, Trapnell BC (2007) PU.1 redirects adenovirus to lysosomes in alveolar macrophages, uncoupling internalization from infection. J Immunol 178: 2440-2447.
67. Peri S, Navarro JD, Amanchy R, Kristiansen TZ, Jonnalagadda CK, et al. (2003) Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res 13: 2363-2371.
68. Alfarano C, Andrade CE, Anthony K, Bahroos N, Bajec M, et al. (2005) The Biomolecular Interaction Network Database and related tools 2005 update. Nucleic Acids Res 33: D418-D424.
69. Barthel R, Tsytsykova AV, Barczak AK, Tsai EY, Dascher CC, et al. (2003) Regulation of tumor necrosis factor alpha gene expression by mycobacteria involves the assembly of a unique enhanceosome dependent on the coactivator proteins CBP/p300. Mol Cell Biol 23: 526-533.
70. Bertolino E, Reimund B, Wildt-Perinic D, Clerc RG (1995) A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J Biol Chem 270: 31178-31188.
71. Bartholin L, Powers SE, Melhuish TA, Lasse S, Weinstein M, et al. (2006) TGIF inhibits retinoid signaling. Mol Cell Biol 26: 990-1001.
72. Hamilton JA (2002) GM-CSF in inflammation and autoimmunity. Trends Immunol 23: 403-408.
73. Nolan KF, Strong V, Soler D, Fairchild PJ, Cobbold SP, et al. (2004) IL-10-conditioned dendritic cells, decomissioned for recruitment of adaptive immunity, elicit innate inflammatory gene products in response to danger signals. J Immunol 172: 2201-2209.
74. Pessah M, Prunier C, Marais J, Ferrand N, Mazars A, et al. (2001) c-Jun interacts with the corepressor TG-interacting factor (TGIF) to suppress Smad2 transcriptional activity. Proc Natl Acad Sci USA 98: 6198-6203.
75. Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85: 461-464.
76. 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.
77. Goldmann O, von Kockritz-Blickwede M, Holtje C, Chhatwal GS, Geffers R, et al. (2007) Transcriptome analysis of murine macrophages in response to infection with Streptococcus pyogenes reveals an unusual activation program. Infection Immunity (online ahead of print).
78. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
79. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
80. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289-300.
81. Affymetrix (2007) Affymetrix Mouse GeneChip 430.2 annotation database, 2007/03/09. Available: http://www.affymetrix.com.
82. Affymetrix (2006) Data Analysis Fundamentals. Available: http://www.affymetrix.com/support/technical/manual/expression_manual.affx.
83. Roach JC, Smith KD, Strobe KL, Nissen SM, Haudenschild CD, et al. (2007) Transcription factor expression in lipopolysaccharide-activated peripheral blood derived mononuclear cells. Proc Natl Acad Sci U S A 104: 16245-16250.
84. Dollar P (2006) Piotr Dollar's Image and Video Toolbox for Matlab (computer program), ver. 1.03. San DiegoCA: University of California, San Diego, Available: http://vision.ucsd.edu/,pdollar/toolbox.
85. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1988) Numerical Recipes in C. New Rochelle, NY: Cambridge University Press.
86. Jackson Laboratory (2006) Mouse Genome Informatics annotations. Available: http://www.jax.org/mgi.
87. Gene Ontology Project (2006) The Gene Ontology (OBO format). Available: http://www.geneontology.org.
88. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99-104.
89. Smit AF, Hubley R, Green P (2007) RepeatMasker software program (computer program), ver. 3.1.8. Seattle: Institute for Systems Biology. Available: http://www.repeatmasker.org.
90. Thijs G, Moreau Y, De Smet F, Mathys J, Lescot M, et al. (2002) INCLUSive: INtegrated Clustering, Upstream sequence retrieval and motif Sampling. Bioinformatics 18: 331-332.
91. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
92. Glesne D, Huberman E (2006) Smad6 is a protein kinase X phosphorylation substrate and is required for HL-60 cell differentiation. Oncogene 25: 4086-4098.
93. Flo TH, Smith KD, Sato S, Rodriguez DJ, Holmes MA, et al. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921.
94. Innate Immunity Systems Biology Project (2006) Innate Immunity Systems Biology - List of Genes Tiled for Promoter Array. Available: http://www.innateimmunity-systemsbiology.org.
95. Affymetrix (2002) Statistical algorithm description document. Available: http://www.affymetrix.com/support/technical/whitepapers.affx.
96. Parkinson H, Kapushesky M, Shojatalab M, Abeygunawardena N, Coulson R, et al. (2007) ArrayExpress - a public database of microarray experiments and gene expression profiles. Nucleic Acids Res 35: D747-D750.