Tumor cell‐specific inhibition of MYC function using small molecule inhibitors of the HUWE1 ubiquitin ligase

Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF‐BP1, MULE) associates with both MYC and the MYC‐associated protein MIZ1. We show here that HUWE1 is required for growth of colorecta...

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Published inEMBO molecular medicine Vol. 6; no. 12; pp. 1525 - 1541
Main Authors Peter, Stefanie, Bultinck, Jennyfer, Myant, Kevin, Jaenicke, Laura A, Walz, Susanne, Müller, Judith, Gmachl, Michael, Treu, Matthias, Boehmelt, Guido, Ade, Carsten P, Schmitz, Werner, Wiegering, Armin, Otto, Christoph, Popov, Nikita, Sansom, Owen, Kraut, Norbert, Eilers, Martin
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.12.2014
John Wiley & Sons, Inc
EMBO Press
BlackWell Publishing Ltd
Springer Nature
Subjects
Animals
Cancer
Carcinogenesis
Cell culture
Cell Line, Tumor
Cell Proliferation
Colon cancer
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms - drug therapy
Colorectal Neoplasms - enzymology
Colorectal Neoplasms - genetics
Colorectal Neoplasms - physiopathology
EMBO03
EMBO12
EMBO28
Epithelial cells
Experiments
Gene expression
Gene Expression Regulation, Neoplastic
Gene silencing
Genetic transcription
Humans
HUWE1
Huwe1 protein
Kruppel-Like Transcription Factors - genetics
Kruppel-Like Transcription Factors - metabolism
Laboratories
Ligases
Mice
Mice, SCID
MIZ1
MYC
Myc protein
Oncogene Protein p55(v-myc) - antagonists & inhibitors
Oncogene Protein p55(v-myc) - genetics
Oncogene Protein p55(v-myc) - metabolism
Protein Binding
Proteins
Research Article
Signal transduction
Small Molecule Libraries - administration & dosage
Small Molecule Libraries - pharmacology
Stem cells
Transcription activation
Transcriptional Activation
Tumor cells
Tumor Suppressor Proteins
Tumorigenesis
Ubiquitin
Ubiquitin-protein ligase
Ubiquitin-Protein Ligases - antagonists & inhibitors
Ubiquitin-Protein Ligases - genetics
Ubiquitin-Protein Ligases - metabolism
ubiquitination
Xenografts
HUWE1
colorectal cancer
ubiquitination
MYC
MIZ1
Online AccessGet full text

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Abstract Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF‐BP1, MULE) associates with both MYC and the MYC‐associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high‐throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC‐dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC‐activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells. Synopsis New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes. HUWE1 is essential for growth of colorectal tumors in vivo and is globally required for expression of MYC target genes. Small‐molecule inhibitors of HUWE1 inhibit expression of MYC target genes in a tumor‐cell specific manner. Inhibition of HUWE1 stabilizes MIZ1 and induces global accumulation of MIZ1 on MYC‐bound target genes. Accumulation of MIZ1 is required for repression of ribosomal protein genes upon HUWE1 inhibition. Graphical Abstract New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes.
AbstractList Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF-BP1, MULE) associates with both MYC and the MYC-associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high-throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC-dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC-activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells.
Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF‐BP1, MULE) associates with both MYC and the MYC‐associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high‐throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC‐dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC‐activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells. Synopsis New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes. HUWE1 is essential for growth of colorectal tumors in vivo and is globally required for expression of MYC target genes. Small‐molecule inhibitors of HUWE1 inhibit expression of MYC target genes in a tumor‐cell specific manner. Inhibition of HUWE1 stabilizes MIZ1 and induces global accumulation of MIZ1 on MYC‐bound target genes. Accumulation of MIZ1 is required for repression of ribosomal protein genes upon HUWE1 inhibition. Graphical Abstract New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes.
Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF-BP1, MULE) associates with both MYC and the MYC-associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high-throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC-dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC-activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells.Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF-BP1, MULE) associates with both MYC and the MYC-associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high-throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC-dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC-activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells.
Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF-BP1, MULE) associates with both MYC and the MYC-associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high-throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC-dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC-activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells. See also: FX Schaub & JL Cleveland (December 2014)
Abstract Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF‐BP1, MULE) associates with both MYC and the MYC‐associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high‐throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC‐dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC‐activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells.
Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1 (HECTH9, ARF‐BP1, MULE) associates with both MYC and the MYC‐associated protein MIZ1. We show here that HUWE1 is required for growth of colorectal cancer cells in culture and in orthotopic xenograft models. Using high‐throughput screening, we identify small molecule inhibitors of HUWE1, which inhibit MYC‐dependent transactivation in colorectal cancer cells, but not in stem and normal colon epithelial cells. Inhibition of HUWE1 stabilizes MIZ1. MIZ1 globally accumulates on MYC target genes and contributes to repression of MYC‐activated target genes upon HUWE1 inhibition. Our data show that transcriptional activation by MYC in colon cancer cells requires the continuous degradation of MIZ1 and identify a novel principle that allows for inhibition of MYC function in tumor cells. Synopsis New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes. HUWE1 is essential for growth of colorectal tumors in vivo and is globally required for expression of MYC target genes. Small‐molecule inhibitors of HUWE1 inhibit expression of MYC target genes in a tumor‐cell specific manner. Inhibition of HUWE1 stabilizes MIZ1 and induces global accumulation of MIZ1 on MYC‐bound target genes. Accumulation of MIZ1 is required for repression of ribosomal protein genes upon HUWE1 inhibition. New highly specific inhibitors of HUWE1 have been identified that can inhibit MYC function in a tumour cell‐specific manner, by preventing the HUWE1‐mediated block of a repressive complex of MYC with MIZ1 on MYC‐activated target genes.
Audience Academic
Author Walz, Susanne
Wiegering, Armin
Sansom, Owen
Jaenicke, Laura A
Boehmelt, Guido
Müller, Judith
Schmitz, Werner
Bultinck, Jennyfer
Popov, Nikita
Treu, Matthias
Peter, Stefanie
Otto, Christoph
Kraut, Norbert
Gmachl, Michael
Myant, Kevin
Ade, Carsten P
Eilers, Martin
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  organization: CRUK Beatson Institute
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Issue 12
Keywords HUWE1
colorectal cancer
ubiquitination
MYC
MIZ1
Language English
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2013; 3
2007; 446
2012; 487
2013; 27
2010; 107
2013; 24
2010
2002; 111
2000; 20
2011; 61
1997; 89
2010; 188
2010; 285
2004; 5
1999; 4
2008; 105
2008; 10
2009; 459
2013; 5
2012; 149
2014; 511
2003; 11
2004; 431
2011; 146
2011; 108
2006; 20
2010; 26
2005; 121
2005; 123
1999; 18
2005; 102
2008; 27
2013; 31
2007; 6
2011; 44
1997; 16
2008; 22
2008; 455
2013; 110
2011; 25
2012; 7
2010; 7
2003; 22
2012; 9
2009; 17
25368331 - EMBO Mol Med. 2014 Dec;6(12):1509-11
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SSID ssj0065618
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Snippet Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1...
Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase HUWE1...
Abstract Deregulated expression of MYC is a driver of colorectal carcinogenesis, necessitating novel strategies to inhibit MYC function. The ubiquitin ligase...
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StartPage 1525
SubjectTerms Animals
Cancer
Carcinogenesis
Cell culture
Cell Line, Tumor
Cell Proliferation
Colon cancer
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms - drug therapy
Colorectal Neoplasms - enzymology
Colorectal Neoplasms - genetics
Colorectal Neoplasms - physiopathology
EMBO03
EMBO12
EMBO28
Epithelial cells
Experiments
Gene expression
Gene Expression Regulation, Neoplastic
Gene silencing
Genetic transcription
Humans
HUWE1
Huwe1 protein
Kruppel-Like Transcription Factors - genetics
Kruppel-Like Transcription Factors - metabolism
Laboratories
Ligases
Mice
Mice, SCID
MIZ1
MYC
Myc protein
Oncogene Protein p55(v-myc) - antagonists & inhibitors
Oncogene Protein p55(v-myc) - genetics
Oncogene Protein p55(v-myc) - metabolism
Protein Binding
Proteins
Research Article
Signal transduction
Small Molecule Libraries - administration & dosage
Small Molecule Libraries - pharmacology
Stem cells
Transcription activation
Transcriptional Activation
Tumor cells
Tumor Suppressor Proteins
Tumorigenesis
Ubiquitin
Ubiquitin-protein ligase
Ubiquitin-Protein Ligases - antagonists & inhibitors
Ubiquitin-Protein Ligases - genetics
Ubiquitin-Protein Ligases - metabolism
ubiquitination
Xenografts
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Title Tumor cell‐specific inhibition of MYC function using small molecule inhibitors of the HUWE1 ubiquitin ligase
URI https://link.springer.com/article/10.15252/emmm.201403927
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Femmm.201403927
https://www.ncbi.nlm.nih.gov/pubmed/25253726
https://www.proquest.com/docview/2290033078
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Volume 6
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