Genome-wide Characterization of miR-34a Induced Changes in Protein and mRNA Expression by a Combined Pulsed SILAC and Microarray Analysis

The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in pr...

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Published inMolecular & cellular proteomics Vol. 10; no. 8; pp. M111 - M111.010462
Main Authors Kaller, Markus, Liffers, Sven-Thorsten, Oeljeklaus, Silke, Kuhlmann, Katja, Röh, Simone, Hoffmann, Reinhard, Warscheid, Bettina, Hermeking, Heiko
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.08.2011
The American Society for Biochemistry and Molecular Biology
Subjects
3' Untranslated regions
Acetylation
Axl protein
Cell Line, Tumor
Cell proliferation
Colorectal cancer
DNA biosynthesis
DNA microarrays
epigenetics
Gene Expression
Gene Expression Profiling
Gene Expression Regulation
Genes, Reporter
Genes, Tumor Suppressor
Genome, Human
Glycolysis
Humans
Isotope Labeling
Lipid metabolism
Luciferases, Renilla - biosynthesis
Luciferases, Renilla - genetics
MCM protein
Metabolic Networks and Pathways - genetics
MicroRNAs - metabolism
MicroRNAs - physiology
Migration
miRNA
Oligonucleotide Array Sequence Analysis
p53 protein
Protein biosynthesis
Proteome - genetics
Proteome - metabolism
proteomics
Replication
RNA, Messenger - genetics
RNA, Messenger - metabolism
Transcription
Translation
Tumor cell lines
Tumor suppressor genes
Tumors
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Abstract The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. ∼19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3′-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis (LDHA), WNT-signaling (LEF1), invasion/migration (AXL) and lipid metabolism (ACSL1, ACSL4). Furthermore, miR-34a may activate p53 by inhibiting its acetylation (MTA2, HDAC1) and degradation (YY1). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.
AbstractList The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. ∼19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3'-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis (LDHA), WNT-signaling (LEF1), invasion/migration (AXL) and lipid metabolism (ACSL1, ACSL4). Furthermore, miR-34a may activate p53 by inhibiting its acetylation (MTA2, HDAC1) and degradation (YY1). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. ∼19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3'-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis (LDHA), WNT-signaling (LEF1), invasion/migration (AXL) and lipid metabolism (ACSL1, ACSL4). Furthermore, miR-34a may activate p53 by inhibiting its acetylation (MTA2, HDAC1) and degradation (YY1). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.
The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. ∼19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3'-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis (LDHA), WNT-signaling (LEF1), invasion/migration (AXL) and lipid metabolism (ACSL1, ACSL4). Furthermore, miR-34a may activate p53 by inhibiting its acetylation (MTA2, HDAC1) and degradation (YY1). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.
The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a -induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. ∼19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3′-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis ( LDHA ), WNT-signaling ( LEF1 ), invasion/migration ( AXL ) and lipid metabolism ( ACSL1, ACSL4 ). Furthermore, miR-34a may activate p53 by inhibiting its acetylation ( MTA2, HDAC1 ) and degradation ( YY1 ). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.
The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal cancer and numerous other tumor types. Here, we combined pulsed SILAC (pSILAC) and microarray analyses to identify miR-34a-induced changes in protein and mRNA expression. pSILAC allowed to quantify the de novo protein synthesis of 1206 proteins after activation of a conditional miR-34a allele in a colorectal cancer cell line. similar to 19% of the detected proteins were differentially regulated, with 113 proteins being down- and 115 up-regulated. The proteins with a miR-34a seed-matching-sequence in the 3'-untranslated region (UTR) of the corresponding mRNA showed a clear bias toward translational repression. Proteins involved in DNA replication, e.g. the MCM proteins, and cell proliferation, were over-represented among indirectly down-regulated proteins lacking a miR-34a seed-match. The decrease in de novo protein synthesis of direct miR-34a targets correlated with reduced levels of the corresponding mRNA in most cases, indicating an interdependence of both types of regulation. In addition, 43 mRNAs encoding proteins not detected by pSILAC were down-regulated after miR-34a expression and contained miR-34a seed-matches. The direct regulation of selected miR-34a target-mRNAs was confirmed using reporter assays. Via down-regulation of the proteins encoded by these mRNAs miR-34a presumably inhibits glycolysis (LDHA), WNT-signaling (LEF1), invasion/migration (AXL) and lipid metabolism (ACSL1, ACSL4). Furthermore, miR-34a may activate p53 by inhibiting its acetylation (MTA2, HDAC1) and degradation (YY1). In summary, miR-34a presumably participates in multiple tumor suppressive pathways by directly and indirectly suppressing the expression of numerous, critical proteins.
ArticleNumber M111.010462
Author Oeljeklaus, Silke
Liffers, Sven-Thorsten
Hoffmann, Reinhard
Kuhlmann, Katja
Warscheid, Bettina
Hermeking, Heiko
Kaller, Markus
Röh, Simone
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  organization: Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University Munich, Thalkirchner Strasse 36, D-80337 Munich, Germany
– sequence: 2
  givenname: Sven-Thorsten
  surname: Liffers
  fullname: Liffers, Sven-Thorsten
  organization: Institute of Pathology, Ruhr-University Bochum, Bürkle-de-la-Camp-Platz 1, D-44789 Bochum, Germany
– sequence: 3
  givenname: Silke
  surname: Oeljeklaus
  fullname: Oeljeklaus, Silke
  organization: Faculty of Biology and BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany
– sequence: 4
  givenname: Katja
  surname: Kuhlmann
  fullname: Kuhlmann, Katja
  organization: Medical Proteome-Center, Ruhr-University Bochum, 44780 Bochum, Germany
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  givenname: Simone
  surname: Röh
  fullname: Röh, Simone
  organization: Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University Munich, Thalkirchner Strasse 36, D-80337 Munich, Germany
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  givenname: Reinhard
  surname: Hoffmann
  fullname: Hoffmann, Reinhard
  organization: Institute of Medical Microbiology, Immunology and Hygene, Technical University Munich, Trogerstr. 30, D-81675 Munich, Germany
– sequence: 7
  givenname: Bettina
  surname: Warscheid
  fullname: Warscheid, Bettina
  organization: Faculty of Biology and BIOSS Centre for Biological Signalling Studies, University of Freiburg, 79104 Freiburg, Germany
– sequence: 8
  givenname: Heiko
  surname: Hermeking
  fullname: Hermeking, Heiko
  email: heiko.hermeking@med.uni-muenchen.de
  organization: Experimental and Molecular Pathology, Institute of Pathology, Ludwig-Maximilians-University Munich, Thalkirchner Strasse 36, D-80337 Munich, Germany
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21566225$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2011 © 2011 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.
2011 by The American Society for Biochemistry and Molecular Biology, Inc. 2011
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Discipline Anatomy & Physiology
Biology
DocumentTitleAlternate Identification of miR-34a Targets
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Both authors contributed equally.
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PublicationTitle Molecular & cellular proteomics
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Snippet The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal...
The gene encoding the miR-34a microRNA is a transcriptional target of the p53 tumor suppressor protein and subject to epigenetic inactivation in colorectal...
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SubjectTerms 3' Untranslated regions
Acetylation
Axl protein
Cell Line, Tumor
Cell proliferation
Colorectal cancer
DNA biosynthesis
DNA microarrays
epigenetics
Gene Expression
Gene Expression Profiling
Gene Expression Regulation
Genes, Reporter
Genes, Tumor Suppressor
Genome, Human
Glycolysis
Humans
Isotope Labeling
Lipid metabolism
Luciferases, Renilla - biosynthesis
Luciferases, Renilla - genetics
MCM protein
Metabolic Networks and Pathways - genetics
MicroRNAs - metabolism
MicroRNAs - physiology
Migration
miRNA
Oligonucleotide Array Sequence Analysis
p53 protein
Protein biosynthesis
Proteome - genetics
Proteome - metabolism
proteomics
Replication
RNA, Messenger - genetics
RNA, Messenger - metabolism
Transcription
Translation
Tumor cell lines
Tumor suppressor genes
Tumors
Title Genome-wide Characterization of miR-34a Induced Changes in Protein and mRNA Expression by a Combined Pulsed SILAC and Microarray Analysis
URI https://dx.doi.org/10.1074/mcp.M111.010462
https://www.ncbi.nlm.nih.gov/pubmed/21566225
https://www.proquest.com/docview/881089379
https://www.proquest.com/docview/907173427
https://pubmed.ncbi.nlm.nih.gov/PMC3149097
Volume 10
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