Identification of Y-box binding protein 1 as a core regulator of MEK/ERK pathway-dependent gene signatures in colorectal cancer cells

Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portrait...

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Published inPLoS genetics Vol. 6; no. 12; p. e1001231
Main Authors Jürchott, Karsten, Kuban, Ralf-Jürgen, Krech, Till, Blüthgen, Nils, Stein, Ulrike, Walther, Wolfgang, Friese, Christian, Kiełbasa, Szymon M, Ungethüm, Ute, Lund, Per, Knösel, Thomas, Kemmner, Wolfgang, Morkel, Markus, Fritzmann, Johannes, Schlag, Peter M, Birchmeier, Walter, Krueger, Tammo, Sperling, Silke, Sers, Christine, Royer, Hans-Dieter, Herzel, Hanspeter, Schäfer, Reinhold
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2010
Public Library of Science (PLoS)
Subjects
Cell Biology
Cell Line, Tumor
Chemical properties
Colorectal cancer
Colorectal Neoplasms - enzymology
Colorectal Neoplasms - genetics
Colorectal Neoplasms - metabolism
Computational Biology/Genomics
DNA binding proteins
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Genes
Genes, Regulator
Genetic aspects
Genetics and Genomics/Cancer Genetics
Genomes
Humans
Integrated approach
Kinases
MAP Kinase Signaling System
Mitogen-Activated Protein Kinase Kinases - genetics
Mitogen-Activated Protein Kinase Kinases - metabolism
Molecular Biology/Bioinformatics
Oncology/Gastrointestinal Cancers
Ontology
Pathology/Molecular Pathology
Physiological aspects
Protein kinases
Proteins
Risk factors
Signal transduction
Y-Box-Binding Protein 1 - genetics
Y-Box-Binding Protein 1 - metabolism
Germany
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Abstract Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogen-activated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y-box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBX1-regulated target genes are involved in executing malignant properties.
AbstractList Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogen-activated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y-box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBX1-regulated target genes are involved in executing malignant properties.
  Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogen-activated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y-box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBX1-regulated target genes are involved in executing malignant properties.
Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogenactivated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y- box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBXI-regulated target genes are involved in executing malignant properties.
Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogen-activated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y-box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBX1-regulated target genes are involved in executing malignant properties. The simultaneous analysis of gene expression in cancer using microarrays is a standard approach for monitoring disease-related modifications involved in tumorigenesis, triggering malignant properties and clinical behavior. However, the factors that drive these alterations most often remain elusive. We sought to identify transcription factors that mediate the transcriptional effects of the receptor tyrosine kinase/RAS oncoprotein pathway, a frequently activated oncogenic signaling system, in cultured colorectal cancer cells. We used an integrated approach combining molecular and functional assays, as well as computational tools, to identify regulatory factors that trigger the alterations of gene expression and modulate cellular growth. We identified the YBX1 protein, a member of the highly conserved family of cold shock domain transcription factors, as a regulator of signaling effects triggered by the RAS cancer gene. Then we assayed the messenger RNA expression of YBX1 and YBX1-responsive target genes by interrogating microarrays, and also expression of the YBX1 protein by immunohistochemistry in colorectal tumors. We found that YBX1 expression is correlated with a bad clinical outcome in colon cancer patients.
Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous candidate genes involved in disease and in factors of predictive, as well as of prognostic, value have been deduced from such molecular portraits, e.g. in cancer. However, mechanistic insights into the regulatory principles governing global transcriptional changes are lagging behind extensive compilations of deregulated genes. To identify regulators of transcriptome alterations, we used an integrated approach combining transcriptional profiling of colorectal cancer cell lines treated with inhibitors targeting the receptor tyrosine kinase (RTK)/RAS/mitogen-activated protein kinase pathway, computational prediction of regulatory elements in promoters of co-regulated genes, chromatin-based and functional cellular assays. We identified commonly co-regulated, proliferation-associated target genes that respond to the MAPK pathway. We recognized E2F and NFY transcription factor binding sites as prevalent motifs in those pathway-responsive genes and confirmed the predicted regulatory role of Y-box binding protein 1 (YBX1) by reporter gene, gel shift, and chromatin immunoprecipitation assays. We also validated the MAPK-dependent gene signature in colorectal cancers and provided evidence for the association of YBX1 with poor prognosis in colorectal cancer patients. This suggests that MEK/ERK-dependent, YBX1-regulated target genes are involved in executing malignant properties. The simultaneous analysis of gene expression in cancer using microarrays is a standard approach for monitoring disease-related modifications involved in tumorigenesis, triggering malignant properties and clinical behavior. However, the factors that drive these alterations most often remain elusive. We sought to identify transcription factors that mediate the transcriptional effects of the receptor tyrosine kinase/RAS oncoprotein pathway, a frequently activated oncogenic signaling system, in cultured colorectal cancer cells. We used an integrated approach combining molecular and functional assays, as well as computational tools, to identify regulatory factors that trigger the alterations of gene expression and modulate cellular growth. We identified the YBX1 protein, a member of the highly conserved family of cold shock domain transcription factors, as a regulator of signaling effects triggered by the RAS cancer gene. Then we assayed the messenger RNA expression of YBX1 and YBX1-responsive target genes by interrogating microarrays, and also expression of the YBX1 protein by immunohistochemistry in colorectal tumors. We found that YBX1 expression is correlated with a bad clinical outcome in colon cancer patients.
Audience Academic
Author Lund, Per
Royer, Hans-Dieter
Kuban, Ralf-Jürgen
Walther, Wolfgang
Schlag, Peter M
Schäfer, Reinhold
Kiełbasa, Szymon M
Birchmeier, Walter
Stein, Ulrike
Knösel, Thomas
Blüthgen, Nils
Sers, Christine
Ungethüm, Ute
Sperling, Silke
Krueger, Tammo
Jürchott, Karsten
Krech, Till
Friese, Christian
Kemmner, Wolfgang
Fritzmann, Johannes
Morkel, Markus
Herzel, Hanspeter
AuthorAffiliation 1 Laboratory of Molecular Tumor Pathology, Universitätsmedizin Berlin, Berlin, Germany
4 Max Delbrück Center for Molecular Medicine, Berlin, Germany
7 Charité Comprehensive Cancer Center, Berlin, Germany
9 Institute of Human Genetics and Anthropology, Heinrich-Heine University Düsseldorf, Düsseldorf, Germany
2 Laboratory of Functional Genomics, Universitätsmedizin Berlin, Berlin, Germany
8 Center of Advanced European Studies and Research, Bonn, Germany
5 Max Planck Institute for Molecular Genetics, Berlin, Germany
University of Pennsylvania, United States of America
6 Institute of Pathology, Friedrich-Schiller-University Jena, Jena, Germany
3 Institute for Theoretical Biology, Humboldt University, Berlin, Germany
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/21170361$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2010 Public Library of Science
Jürchott et al. 2010
2010 Jürchott et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Jürchott K, Kuban R-J, Krech T, Blüthgen N, Stein U, et al. (2010) Identification of Y-Box Binding Protein 1 As a Core Regulator of MEK/ERK Pathway-Dependent Gene Signatures in Colorectal Cancer Cells. PLoS Genet 6(12): e1001231. doi:10.1371/journal.pgen.1001231
Copyright_xml – notice: COPYRIGHT 2010 Public Library of Science
– notice: Jürchott et al. 2010
– notice: 2010 Jürchott et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Jürchott K, Kuban R-J, Krech T, Blüthgen N, Stein U, et al. (2010) Identification of Y-Box Binding Protein 1 As a Core Regulator of MEK/ERK Pathway-Dependent Gene Signatures in Colorectal Cancer Cells. PLoS Genet 6(12): e1001231. doi:10.1371/journal.pgen.1001231
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DocumentTitleAlternate YBX1 and MEK/ERK-Gene Signatures in Colon Cancer
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Conceived and designed the experiments: K Jürchott, H Herzel, R Schäfer. Performed the experiments: K Jürchott, T Krech, U Stein, W Walther, C Friese, U Ungethüm, P Lund, T Knösel, W Kemmner, M Morkel. Analyzed the data: K Jürchott, RJ Kuban, N Blüthgen, U Stein, W Walther, SM Kielbasa, T Knösel, W Kemmner, J Fritzmann, T Krueger, S Sperling, C Sers, H Herzel, R Schäfer. Contributed reagents/materials/analysis tools: K Jürchott, N Blüthgen, M Morkel, J Fritzmann, PM Schlag, W Birchmeier, C Sers, HD Royer. Wrote the paper: K Jürchott, N Blüthgen, R Schäfer.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2996331/
PMID 21170361
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PublicationTitle PLoS genetics
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Snippet Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous...
  Transcriptional signatures are an indispensible source of correlative information on disease-related molecular alterations on a genome-wide level. Numerous...
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SubjectTerms Cell Biology
Cell Line, Tumor
Chemical properties
Colorectal cancer
Colorectal Neoplasms - enzymology
Colorectal Neoplasms - genetics
Colorectal Neoplasms - metabolism
Computational Biology/Genomics
DNA binding proteins
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Neoplastic
Genes
Genes, Regulator
Genetic aspects
Genetics and Genomics/Cancer Genetics
Genomes
Humans
Integrated approach
Kinases
MAP Kinase Signaling System
Mitogen-Activated Protein Kinase Kinases - genetics
Mitogen-Activated Protein Kinase Kinases - metabolism
Molecular Biology/Bioinformatics
Oncology/Gastrointestinal Cancers
Ontology
Pathology/Molecular Pathology
Physiological aspects
Protein kinases
Proteins
Risk factors
Signal transduction
Y-Box-Binding Protein 1 - genetics
Y-Box-Binding Protein 1 - metabolism
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Title Identification of Y-box binding protein 1 as a core regulator of MEK/ERK pathway-dependent gene signatures in colorectal cancer cells
URI https://www.ncbi.nlm.nih.gov/pubmed/21170361
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http://dx.doi.org/10.1371/journal.pgen.1001231
Volume 6
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