Extracting regulator activity profiles by integration of de novo motifs and expression data: Characterizing key regulators of nutrient depletion responses in Streptomyces coelicolor

Nucleic Acids Research

Volumn 40, Issue 12, 2012, Pages 5227-5239

  Iqbal, Mudassar ^a   Mast, Yvonne ^b   Amin, Rafat ^b   Hodgson, David A ^c   Wohlleben, Wolfgang ^b   Burroughs, Nigel J ^d  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LEXA PROTEIN; PHOP PROTEIN; PROTEIN SARP; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BINDING SITE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE SEQUENCE; GENETIC CONSERVATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; SENSITIVITY ANALYSIS; STREPTOMYCES COELICOLOR; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENOMICS; GLUTAMIC ACID; NUCLEOTIDE MOTIFS; PHOSPHATES; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

ESCHERICHIA COLI; STREPTOMYCES COELICOLOR;

EID: 84863201496     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks205     Document Type: Article

References (53)

1. Ross,P.L., Huang,Y.N., Marchese,J.N., Williamson,B., Parker,K., Hattan,S., Khainovski,N., Pillai,S., Dey,S., Daniels,S. et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics, 3, 1154-1169.
2. Shadforth,I.P., Dunkley,T.P.J., Lilley,K.S. and Bessant,C. (2005) i-Tracker: for quantitative proteomics using iTRAQ. BMC Genomics, 6, 145, doi:10.1186/1471-2164-6-145.
3. Gao,F., Foat,B.C. and Bussemaker,H.J. (2004) Defining transcriptional networks through integrative modeling of mRNA expression and transcription factor binding data. BMC Bioinformtics, 5, doi:10.1186/1471-2105-5-31.
4. Ucar,D., Beyer,A., Parthasarathy,S. and Workman,C.T. (2009) Predicting functionality of protein-DNA interactions by integrating diverse evidence. Bioinformatics, 25, i137-i144.
5. Liao,J., Boscolo,R., Yang,Y., Tran,L.M., Sabatti,C. and Roychowdhury,V.P. (2003) Network component analysis: reconstruction of regulatory signals in biological systems. PNAS, 100, 15522-15527. (Pubitemid 38021022)
6. Sabatti,C. and James,G.M. (2006) Bayesian sparse hidden components analysis for transcription regulation networks. Bioinformatics, 22, 739-746.
7. Sanguinetti,G., Lawrence,N.D. and Rattray,M. (2006) Probabilistic inference of transcription factor concentrations and gene-specific regulatory activities. Bioinformatics, 22, 2775-2781. (Pubitemid 44742398)
8. Honkela,A., Girardot,C., Gustafson,E.H., Liu,Y.H., Furlong,E.E., Lawrence,N.D. and Rattray,M. (2010) Model-based method for transcription factor target identification with limited data. Proc. Natl Acad. Sci. USA, 107, 7793-7798.
9. Khanin,R., Vinciotti,V., Mersinias,V., Smith,C.P. and Wit,E. (2007) Statistical reconstruction of transcription factor activity using Michaelis-Menten kinetics. Biometrics, 63, 816-823. (Pubitemid 47352836)
10. Pournara,I. and Wernisch,L. (2007) Factor analysis for gene regulatory networks and transcription factor activity profiles. BMC Bioinformatics, 8, 61.
11. Martín,J.F. and Liras,P. (2010) Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr. Opin. Microbiol., 13, 263-273.
12. Rokem,J.S., Lantz,A.E. and Nielsen,J. (2007) Systems biology of antibiotic production by microorganisms. Natural Prod. Rep., 24, 1262-1287. (Pubitemid 350153625)
13. Novotna,J., Vohradsky,J., Berndt,P., Gramajo,H., Langen,H., Li,X.M., Minas,W., Orsaria,L., Roeder,D. and Thompson,C.J. (2003) Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol Microbiol., 48, 1289-1303. (Pubitemid 36718223)
14. Sola-Landa,A., Rodríguez-García,A., Apel,A.K. and Martín,J.F. (2008) Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor. Nucleic Acids Res., 36, 1358-1368. (Pubitemid 351330950)
15. Rodríuez-García,A., Sola-Landa,A., Apel,A.K., Santos-Beneit,F. and Martín,J.F. (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res., 37, 3230-3242.
16. Rodríguez-García,A., Barreiro,C., Santos-Beneit,F., Sola-Landa,A. and Martín,J.F. (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics, 7, 2410-2429.
17. Rigali,S., Titgemeyer,F., Barends,S., Mulder,S., Thomae,A.W., Hopwood,D.A. and van Wezel,G.P. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep., 9, 670-675. (Pubitemid 351927688)
18. Folcher,M., Gaillard,H., Nguyen,L.T., Nguyen,K.T., Lacroix,P., Bamas-Jacques,N., Rinkel,M. and Thompson,C.J. (2001) Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J. Biol. Chem., 276, 44297-44306.
19. Wietzorrek,A. and Bibb,M. (1997) A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold. Mol. Microbiol., 25, 1177-1184.
20. Sheldon,P.J., Busarow,S.B. and Hutchinson,C.R. (2002) Mapping the DNA-binding domain and target sequences of the Streptomyces peucetius daunorubicin biosynthesis regulatory protein, DnrI. Mol. Microbiol., 44, 449-460. (Pubitemid 34429747)
21. Ran RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J., 17, 5776-5782.
22. Reuther,J. and Wohlleben,W. (2007) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J. Mol. Microbiol. Biotechnol., 12, 139-146. (Pubitemid 46011135)
23. Touzain,F., Schbath,S., Debled-Rennesson,I., Aigle,B., Kucherov,G. and Leblond,P. (2008) SIGffRid: a tool to search for sigma factor binding sites in bacterial genomes using comparative approach and biologically driven statistics. BMC Bioinformatics, 9, 73.
24. Studholme,D.J., Bentley,S.D. and Kormanec,J. (2004) Bioinformatic identification of novel regulatory DNA sequence motifs in Streptomyces coelicolor. BMC Microbiology, 4, 14.
25. Li,H., Rhodius,V., Gross,C. and Siggia,E.D. (2002) Identification of the binding sites of regulatory proteins in bacterial genomes. Proc. Natl. Acad. Sci. USA, 99, 11772-11777. (Pubitemid 34994474)
26. Robison,K., McGuire,A.M. and Church,G.M. (1998) A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. J. Mol. Biol., 284, 241-254. (Pubitemid 28542451)
27. Nieselt,K., Battke,F., Herbig,A., Bruheim,P., Wentzel,A., Jakobsen,Ø.M., Sletta,H., Alam,M.T., Merlo,M.E., Moore,J. et al. (2010) The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics, 11, doi:10.1186/1471-2164-11-10.
28. Waldvogel,E., Herbig,A., Battke,F., Amin,R., Nentwich,M., Nieselt,K., Ellingsen,T.E., Wentzel,A., Hodgson,D.A., Wohlleben,W. et al. (2011) The PIIprotein GlnK is a pleiotropic regulator for morphological differentiation and secondary metabolism in Streptomyces coelicolor. Appl. Microbiol. Biotechnol., 92, 1219-1236.
29. Angelini,C., Cutillo,L., De Canditiis,D., Mutarelli,M. and Pensky,M. (2008) BATS: a Bayesian user-friendly software for Analyzing Time Series microarray experiments. BMC Bioinformatics, 9, 145.
30. Heard,N.A., Holmes,C.C. and Stephens,D.A. (2006) A quantitative study of gene regulation involved in the immune response of Anopheline mosquitoes: an application of Bayesian hierarchical clustering of curves. J. Amer. Stat. Assoc., 101, 18-29. (Pubitemid 43500022)
31. Bentley,S.D., Chater,K.F., Cerdeño-Tárraga,A.M., Challis,G.L., Thomson,N.R., James,K.D., Harris,D.E., Quail,M.A., Kieser,H., Harper,D. et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature, 417, 141-147. (Pubitemid 34506788)
32. Charaniya,S., Mehra,S., Lian,W., Jayapal,K.P., Karypis,G. and Hu,W. (2007) Transcriptome dynamics-based operon prediction and verification in Streptomyces coelicolor. Nucleic Acids Res., 35, 7222-7236.
33. Kieser,T., Bibb,M.J., Buttner,M.J., Chater,K.F. and Hopwood,D.A. (2000) Practical Streptomyces Genetics. John Innes Foundation, Norwich.
34. Barrell,D., Dimmer,E., Huntley,R.P., Binns,D., O'Donovan,C. and Apweiler,R. (2009) The GOA database in 2009-an integrated Gene Ontology Annotation resource. Nucleic Acids Res., 37, D396-D403.
35. Crooks,G.E., Hon,G., Chandonia,J.M. and Brenner,S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190. (Pubitemid 38811555)
36. Bailey,T.L. and Elkan,C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In: Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology. AAAI Press, Menlo Park, California, pp. 28-36.
37. Mahony,S. and Benos,P.V. (2007) STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res., 35, W253-W258.
38. Barona-Gómez,F., Lautru,S., Francou,F.X., Leblond,P., Pernodet,J.L. and Challis,G.L. (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology, 152, 3355-3366. (Pubitemid 44734338)
39. R regulon of Streptomyces coelicolor A3(2) reveals a key role in protein quality control during disulphide stress. Microbiology, 156, 1661-1672.
40. Schinko,E., Schad,K., Eys,S., Keller,U. and Wohlleben,W. (2009) Phosphinothricin-tripeptide biosynthesis: an original version of bacterial secondary metabolism? Phytochemistry, 70, 1787-1800.
41. Amir,A., Meshner,S., Beatus,T. and Stavans,J. (2010) Damped oscillations in the adaptive response of the iron homeostasis network of E. coli. Mol. Microbiol., 76, 428-436.
42. Hahn,J.S., Oh,S.Y. and Roe,J.H. (2000) Regulation of the furA and catC operon, encoding a ferric uptake regulator homologue and catalase-peroxidase, respectively, in Streptomyces coelicolor A3(2). J. Bacteriol., 182, 3767-3774.
43. Körner,H., Sofia,H.J. and Zumft,W.G. (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol. Rev., 27, 559-592. (Pubitemid 37456858)
44. Lian,W., Jayapal,K.P., Charaniya,S., Mehra,S., Glod,F., Kyung,Y.S., Sherman,D.H. and Hu,W.S. (2008) Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2). BMC Genomics, 9, 56.
45. Zwir,I., Huang,H. and Groisman,E.A. (2005) Analysis of differentially-regulated genes within a regulatory network by GPS genome navigation. Bioinformatics, 21, 4073-4083. (Pubitemid 41672096)
46. Okanishi,M., Suzuki,K. and Umezawa,H. (1974) Formation and reversion of streptomycetes protoplasts: cultural condition and morphological study. J. Gen. Micro., 80, 389-400.
47. Claessen,D., Rink,R., de Jong,W., Siebring,J., de Vreugd,P., Boersma,F.G., Dijkhuizen,L. and Wosten,H.A. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev., 17, 1714-1726. (Pubitemid 36870335)
48. Thompson,J.D., Higgins,D.G. and Gibson,T.J. (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680. (Pubitemid 24354800)
49. Benjamini,Y. and Hochberg,Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Series B (Methodological), 57, 289-300.
50. Gilks,W.R. and Roberts,G.O. (1996) Strategies for improving MCMC. In: Gilks,W.R., Richardson,S. and Spiegelhalter. (eds), Markov chain Monte Carlo in Practice. Chapman and Hall, London, pp. 89-114.
51. Geyer,C.J. (1991) Markov chain Monte Carlo maximum likelihood. In: Keramidas. (ed.), Computing Science and Statistics: Proceedings of the 23rd Symposium on the Interface. Interface Foundation, Fairfax Station, pp. 156-163.
52. Altekar,G., Dwarkadas,S., Huelsenbeck,J.P. and Ronquist,F. (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20, 407-415. (Pubitemid 38262773)
53. Patzer,S.I. and Hantke,K. (2000) The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J. Biol. Chem., 275, 24321-24332. (Pubitemid 30626521)