A comprehensive map of genome-wide gene regulation in Mycobacterium tuberculosis

Turkarslan, Serdar; Peterson, Eliza R.; Rustad, Tige R.; Minch, Kyle J.; Reiss, David J.; Morrison, Robert; Ma, Shuyi; Price, Nathan D.; Sherman, David R.; Baliga, Nitin S.

doi:10.1038/sdata.2015.10

A comprehensive map of genome-wide gene regulation in Mycobacterium tuberculosis

Journal Article · Tue Mar 31 00:00:00 EDT 2015 · Scientific Data

DOI:https://doi.org/10.1038/sdata.2015.10· OSTI ID:1624540

Turkarslan, Serdar ^[1]; Peterson, Eliza R. ^[2]; Rustad, Tige R. ^[3]; Minch, Kyle J. ^[4]; Reiss, David J. ^[2]; Morrison, Robert ^[4]; Ma, Shuyi ^[5]; Price, Nathan D. ^[2]; Sherman, David R. ^[6]; Baliga, Nitin S. ^[7]

Inst. for Systems Biology, Seattle, WA (United States); DOE/OSTI
Inst. for Systems Biology, Seattle, WA (United States)
Seattle Biomedical Research Institute, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States). Dept. of Global Health, Interdisciplinary Program of Pathobiology
Seattle Biomedical Research Institute, Seattle, WA (United States)
Inst. for Systems Biology, Seattle, WA (United States); Seattle Biomedical Research Institute, Seattle, WA (United States); Univ. of Illinois at Urbana-Champaign, IL (United States). Dept. of Chemical and Biomolecular Engineering
Seattle Biomedical Research Institute, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States). Dept. of Global Health, Interdisciplinary Program of Pathobiology; Univ. of Washington, Seattle, WA (United States). Molecular and Cellular Biology Program
Inst. for Systems Biology, Seattle, WA (United States); Univ. of Washington, Seattle, WA (United States). Molecular and Cellular Biology Program; Univ. of Washington, Seattle, WA (United States). Depts. of Biology and Microbiology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Mycobacterium tuberculosis (MTB) is a pathogenic bacterium responsible for 12 million active cases of tuberculosis (TB) worldwide. The complexity and critical regulatory components of MTB pathogenicity are still poorly understood despite extensive research efforts. In this study, we constructed the first systems-scale map of transcription factor (TF) binding sites and their regulatory target proteins in MTB. We constructed FLAG-tagged overexpression constructs for 206 TFs in MTB, used ChIP-seq to identify genome-wide binding events and surveyed global transcriptomic changes for each overexpressed TF. Here we present data for the most comprehensive map of MTB gene regulation to date. We also define elaborate quality control measures, extensive filtering steps, and the gene-level overlap between ChIP-seq and microarray datasets. Further, we describe the use of TF overexpression datasets to validate a global gene regulatory network model of MTB and describe an online source to explore the datasets.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1624540

Journal Information:: Scientific Data, Journal Name: Scientific Data Journal Issue: 1 Vol. 2; ISSN 2052-4463

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

The Mtb Proteome Library: A Resource of Assays to Quantify the Complete Proteome of Mycobacterium tuberculosis Schubert, Olga T.; Mouritsen, Jeppe; Ludwig, Christina Cell Host & Microbe, Vol. 13, Issue 5 https://doi.org/10.1016/j.chom.2013.04.008	journal	May 2013
Architectural plan of transcriptional regulation in Mycobacterium tuberculosis Baloni, Priyanka; Chandra, Nagasuma Trends in Microbiology, Vol. 23, Issue 3 https://doi.org/10.1016/j.tim.2015.02.002	journal	March 2015
TubercuList – 10 years after Lew, Jocelyne M.; Kapopoulou, Adamandia; Jones, Louis M. Tuberculosis, Vol. 91, Issue 1 https://doi.org/10.1016/j.tube.2010.09.008	journal	January 2011
The Mycobacterium tuberculosis regulatory network and hypoxia Galagan, James E.; Minch, Kyle; Peterson, Matthew Nature, Vol. 499, Issue 7457 https://doi.org/10.1038/nature12337	journal	July 2013
Design and analysis of ChIP-seq experiments for DNA-binding proteins Kharchenko, Peter V.; Tolstorukov, Michael Y.; Park, Peter J. Nature Biotechnology, Vol. 26, Issue 12 https://doi.org/10.1038/nbt.1508	journal	November 2008
Wisdom of crowds for robust gene network inference Marbach, Daniel; Costello, James C.; Küffner, Robert Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2016	journal	July 2012
Proteomic Profiling of Mycobacterium tuberculosis Identifies Nutrient-starvation-responsive Toxin–antitoxin Systems Albrethsen, Jakob; Agner, Jeppe; Piersma, Sander R. Molecular & Cellular Proteomics, Vol. 12, Issue 5 https://doi.org/10.1074/mcp.m112.018846	journal	January 2013
RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis Hong, Fangxin; Breitling, Rainer; McEntee, Connor W. Bioinformatics, Vol. 22, Issue 22 https://doi.org/10.1093/bioinformatics/btl476	journal	September 2006
An HMM approach to genome-wide identification of differential histone modification sites from ChIP-seq data Xu, Han; Wei, Chia-Lin; Lin, Feng Bioinformatics, Vol. 24, Issue 20 https://doi.org/10.1093/bioinformatics/btn402	journal	July 2008
POLYPHEMUS: R package for comparative analysis of RNA polymerase II ChIP-seq profiles by non-linear normalization Mendoza-Parra, Marco A.; Sankar, Martial; Walia, Mannu Nucleic Acids Research, Vol. 40, Issue 4 https://doi.org/10.1093/nar/gkr1205	journal	December 2011
KEGG for integration and interpretation of large-scale molecular data sets Kanehisa, M.; Goto, S.; Sato, Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr988	journal	November 2011
NCBI GEO: archive for functional genomics data sets—update Barrett, Tanya; Wilhite, Stephen E.; Ledoux, Pierre Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1193	journal	November 2012
GenBank Benson, Dennis A.; Cavanaugh, Mark; Clark, Karen Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1195	journal	November 2012
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases Caspi, Ron; Altman, Tomer; Billington, Richard Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1103	journal	November 2013
Network portal: a database for storage, analysis and visualization of biological networks Turkarslan, Serdar; Wurtmann, Elisabeth J.; Wu, Wei-Ju Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1190	journal	November 2013
STRING v10: protein–protein interaction networks, integrated over the tree of life Szklarczyk, Damian; Franceschini, Andrea; Wyder, Stefan Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1003	journal	October 2014
A high-resolution network model for global gene regulation in Mycobacterium tuberculosis Peterson, Eliza J. R.; Reiss, David J.; Turkarslan, Serdar Nucleic Acids Research, Vol. 42, Issue 18 https://doi.org/10.1093/nar/gku777	journal	September 2014
UniProt: a hub for protein information Consortium, UniPot Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212 https://doi.org/10.1093/nar/gku989	journal	October 2014
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Hypoxia: a window into Mycobacterium tuberculosis latency Rustad, Tige R.; Sherrid, Ashley M.; Minch, Kyle J. Cellular Microbiology, Vol. 11, Issue 8 https://doi.org/10.1111/j.1462-5822.2009.01325.x	journal	August 2009
PeakRanger: A cloud-enabled peak caller for ChIP-seq data Feng, Xin; Grossman, Robert; Stein, Lincoln BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-139	journal	May 2011
ChIP-seq Analysis in R (CSAR): An R package for the statistical detection of protein-bound genomic regions Muiño, Jose M.; Kaufmann, Kerstin; van Ham, Roeland CHJ Plant Methods, Vol. 7, Issue 1 https://doi.org/10.1186/1746-4811-7-11	journal	January 2011
The need for speed Flicek, Paul Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-212	journal	January 2009
Mapping and manipulating the Mycobacterium tuberculosis transcriptome using a transcription factor overexpression-derived regulatory network Rustad, Tige R.; Minch, Kyle J.; Ma, Shuyi Genome Biology, Vol. 15, Issue 11 https://doi.org/10.1186/s13059-014-0502-3	journal	November 2014
Large-Scale Mapping and Validation of Escherichia coli Transcriptional Regulation from a Compendium of Expression Profiles Faith, Jeremiah J.; Hayete, Boris; Thaden, Joshua T. PLoS Biology, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pbio.0050008	journal	January 2007
The Enduring Hypoxic Response of Mycobacterium tuberculosis Rustad, Tige R.; Harrell, Maria I.; Liao, Reiling PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001502	journal	January 2008
Mycobacterium tuberculosis Growth following Aerobic Expression of the DosR Regulon Minch, Kyle; Rustad, Tige; Sherman, David R. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035935	journal	April 2012
Transcriptional Profiling of Mycobacterium tuberculosis Replicating Ex vivo in Blood from HIV- and HIV+ Subjects Ryndak, Michelle B.; Singh, Krishna K.; Peng, Zhengyu PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0094939	journal	April 2014
High-Resolution Phenotypic Profiling Defines Genes Essential for Mycobacterial Growth and Cholesterol Catabolism Griffin, Jennifer E.; Gawronski, Jeffrey D.; DeJesus, Michael A. PLoS Pathogens, Vol. 7, Issue 9 https://doi.org/10.1371/journal.ppat.1002251	journal	September 2011
A comprehensive map of genome-wide gene regulation in Mycobacterium tuberculosis Turkarslan, Serdar figshare https://doi.org/10.6084/m9.figshare.1249805.v1	dataset	January 2014
limma: Linear Models for Microarray Data Smyth, G. K. Bioinformatics and Computational Biology Solutions Using R and Bioconductor https://doi.org/10.1007/0-387-29362-0_23	book	January 2005
Comparative Genomic Analysis at the PATRIC, A Bioinformatic Resource Center Wattam, Alice R.; Gabbard, Joseph L.; Shukla, Maulik Host-Bacteria Interactions https://doi.org/10.1007/978-1-4939-1261-2_17	book	January 2014
Genome-wide Mapping of Transcriptional Start Sites Defines an Extensive Leaderless Transcriptome in Mycobacterium tuberculosis Cortes, Teresa; Schubert, Olga T.; Rose, Graham Cell Reports, Vol. 5, Issue 4 https://doi.org/10.1016/j.celrep.2013.10.031	journal	November 2013
TB database 2010: Overview and update Galagan, James E.; Sisk, Peter; Stolte, Christian Tuberculosis, Vol. 90, Issue 4 https://doi.org/10.1016/j.tube.2010.03.010	journal	July 2010
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
The DNA-binding network of Mycobacterium tuberculosi s Minch, Kyle J.; Rustad, Tige R.; Peterson, Eliza J. R. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms6829	journal	January 2015
A computational pipeline for comparative ChIP-seq analyses Bardet, Anaïs F.; He, Qiye; Zeitlinger, Julia Nature Protocols, Vol. 7, Issue 1 https://doi.org/10.1038/nprot.2011.420	journal	December 2011
Spatiotemporal persistence of multiple, diverse clades and toxins of Corynebacterium diphtheriae Will, Robert C.; Ramamurthy, Thandavarayan; Sharma, Naresh Chand Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21870-5	journal	March 2021
SPOCD1 is an essential executor of piRNA-directed de novo DNA methylation Zoch, Ansgar; Auchynnikava, Tania; Berrens, Rebecca V. Nature, Vol. 584, Issue 7822 https://doi.org/10.1038/s41586-020-2557-5	journal	July 2020
inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains Olm, Matthew R.; Crits-Christoph, Alexander; Bouma-Gregson, Keith Nature Biotechnology, Vol. 39, Issue 6 https://doi.org/10.1038/s41587-020-00797-0	journal	January 2021
Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling: Nutrient starvation of M. tuberculosis Betts, Joanna C.; Lukey, Pauline T.; Robb, Linda C. Molecular Microbiology, Vol. 43, Issue 3 https://doi.org/10.1046/j.1365-2958.2002.02779.x	journal	February 2002
Genes required for mycobacterial growth defined by high density mutagenesis: Genes required for mycobacterial growth Sassetti, Christopher M.; Boyd, Dana H.; Rubin, Eric J. Molecular Microbiology, Vol. 48, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03425.x	journal	March 2003
Dynamic antibody responses to the Mycobacterium tuberculosis proteome Kunnath-Velayudhan, S.; Salamon, H.; Wang, H. -Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1009080107	journal	July 2010
Proteomic Profiling of Mycobacterium tuberculosis Identifies Nutrient-starvation-responsive Toxin–antitoxin Systems Albrethsen, Jakob; Agner, Jeppe; Piersma, Sander R. Molecular & Cellular Proteomics, Vol. 12, Issue 5 https://doi.org/10.1074/mcp.M112.018846	journal	January 2013
Characterization and Transcriptome Analysis of Mycobacterium tuberculosis Persisters Keren, Iris; Minami, Shoko; Rubin, Eric mBio, Vol. 2, Issue 3 https://doi.org/10.1128/mBio.00100-11	journal	June 2011
The COG database: an updated version includes eukaryotes Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D. BMC Bioinformatics, Vol. 4, Article No. 41 https://doi.org/10.1186/1471-2105-4-41	journal	January 2003
Mapping and manipulating the Mycobacterium tuberculosis transcriptome using a transcription factor overexpression-derived regulatory network Rustad, Tige R.; Minch, Kyle J.; Ma, Shuyi Genome Biology, Vol. 15, Issue 11 https://doi.org/10.1186/PREACCEPT-1701638048134699	journal	January 2014
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
The Mtb Proteome Library: A Resource of Assays to Quantify the Complete Proteome of Mycobacterium tuberculosis Schubert, Olga T.; Mouritsen, Jeppe; Ludwig, Christina ETH Zurich https://doi.org/10.3929/ethz-b-000078102	text	January 2013
Genome-wide Mapping of Transcriptional Start Sites Defines an Extensive Leaderless Transcriptome in Mycobacterium tuberculosis Cortes, Teresa; Schubert, Olga T.; Rose, Graham ETH Zurich https://doi.org/10.3929/ethz-b-000079344	text	January 2013
A comprehensive map of genome-wide gene regulation in Mycobacterium tuberculosis Turkarslan, Serdar figshare https://doi.org/10.6084/m9.figshare.1249805	dataset	January 2014

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Comparative ‘omics analyses differentiate Mycobacterium tuberculosis and Mycobacterium bovis and reveal distinct macrophage responses to infection with the human and bovine tubercle bacilli Malone, Kerri M.; Rue-Albrecht, Kévin; Magee, David A. Microbial Genomics https://doi.org/10.1101/220624	posted_content	November 2017
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Gene Enrichment Analysis Reveals Major Regulators of Mycobacterium tuberculosis Gene Expression in Two Models of Antibiotic Tolerance Matern, William M.; Rifat, Dalin; Bader, Joel S. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00610	journal	April 2018
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