Pharmacological targeting of MYC-regulated IRE1/XBP1 pathway suppresses MYC-driven breast cancer

The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that...

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Published inThe Journal of clinical investigation Vol. 128; no. 4; pp. 1283 - 1299
Main Authors Zhao, Na, Cao, Jin, Xu, Longyong, Tang, Qianzi, Dobrolecki, Lacey E., Lv, Xiangdong, Talukdar, Manisha, Lu, Yang, Wang, Xiaoran, Hu, Dorothy Z., Shi, Qing, Xiang, Yu, Wang, Yunfei, Liu, Xia, Bu, Wen, Jiang, Yi, Li, Mingzhou, Gong, Yingyun, Sun, Zheng, Ying, Haoqiang, Yuan, Bo, Lin, Xia, Feng, Xin-Hua, Hartig, Sean M., Li, Feng, Shen, Haifa, Chen, Yiwen, Han, Leng, Zeng, Qingping, Patterson, John B., Kaipparettu, Benny Abraham, Putluri, Nagireddy, Sicheri, Frank, Rosen, Jeffrey M., Lewis, Michael T., Chen, Xi
Format Journal Article
LanguageEnglish
Published United States American Society for Clinical Investigation 01.04.2018
Subjects
Activating transcription factor 1
Animal models
Animals
Biomedical research
Breast cancer
Breast Neoplasms - drug therapy
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer therapies
Cancer treatment
Care and treatment
Cell Line, Tumor
Chemotherapy
Development and progression
Docetaxel - pharmacology
Drug Delivery Systems
Endoplasmic reticulum
Endoribonucleases - genetics
Endoribonucleases - metabolism
Enzymes
Female
Genes
Genetic aspects
Genetic engineering
Health aspects
Humans
Inositol
Kinases
Mice
Molecular modelling
Myc protein
Nucleotidases
Pharmacological research
Phosphorylation
Physiological aspects
Protein folding
Protein-Serine-Threonine Kinases - genetics
Protein-Serine-Threonine Kinases - metabolism
Proteins
Proto-Oncogene Proteins c-myc - genetics
Proto-Oncogene Proteins c-myc - metabolism
Response Elements
Ribonuclease
Saccharomyces cerevisiae
Signal Transduction - drug effects
Signal Transduction - genetics
Stem cells
Transcription
Transcription factors
Tumors
Unfolded Protein Response - drug effects
Unfolded Protein Response - genetics
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
Xenograft Model Antitumor Assays
Xenografts
United States > US
Oncology
Breast cancer
Cell stress
Drug therapy
Therapeutics
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Abstract The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that oncogenic MYC regulates the inositol-requiring enzyme 1 (IRE1)/X-box binding protein 1 (XBP1) branch of the UPR in breast cancer via multiple mechanisms. We found that MYC directly controls IRE1 transcription by binding to its promoter and enhancer. Furthermore, MYC forms a transcriptional complex with XBP1, a target of IRE1, and enhances its transcriptional activity. Importantly, we demonstrate that XBP1 is a synthetic lethal partner of MYC. Silencing of XBP1 selectively blocked the growth of MYC-hyperactivated cells. Pharmacological inhibition of IRE1 RNase activity with small molecule inhibitor 8866 selectively restrained the MYC-overexpressing tumor growth in vivo in a cohort of preclinical patient-derived xenograft models and genetically engineered mouse models. Strikingly, 8866 substantially enhanced the efficacy of docetaxel chemotherapy, resulting in rapid regression of MYC-overexpressing tumors. Collectively, these data establish the synthetic lethal interaction of the IRE1/XBP1 pathway with MYC hyperactivation and provide a potential therapy for MYC-driven human breast cancers.
AbstractList The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that oncogenic MYC regulates the inositol-requiring enzyme 1 (IRE1)/X-box binding protein 1 (XBP1) branch of the UPR in breast cancer via multiple mechanisms. We found that MYC directly controls IRE1 transcription by binding to its promoter and enhancer. Furthermore, MYC forms a transcriptional complex with XBP1, a target of IRE1, and enhances its transcriptional activity. Importantly, we demonstrate that XBP1 is a synthetic lethal partner of MYC. Silencing of XBP1 selectively blocked the growth of MYC-hyperactivated cells. Pharmacological inhibition of IRE1 RNase activity with small molecule inhibitor 8866 selectively restrained the MYC-overexpressing tumor growth in vivo in a cohort of preclinical patient-derived xenograft models and genetically engineered mouse models. Strikingly, 8866 substantially enhanced the efficacy of docetaxel chemotherapy, resulting in rapid regression of MYC-overexpressing tumors. Collectively, these data establish the synthetic lethal interaction of the IRE1/XBP1 pathway with MYC hyperactivation and provide a potential therapy for MYC-driven human breast cancers.
The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that oncogenic MYC regulates the inositol-requiring enzyme 1 (IRE1)/X-box binding protein 1 (XBP1) branch of the UPR in breast cancer via multiple mechanisms. We found that MYC directly controls IRE1 transcription by binding to its promoter and enhancer. Furthermore, MYC forms a transcriptional complex with XBP1, a target of IRE1, and enhances its transcriptional activity. Importantly, we demonstrate that XBP1 is a synthetic lethal partner of MYC. Silencing of XBP1 selectively blocked the growth of MYC-hyperactivated cells. Pharmacological inhibition of IRE1 RNase activity with small molecule inhibitor 8866 selectively restrained the MYC-overexpressing tumor growth in vivo in a cohort of preclinical patient-derived xenograft models and genetically engineered mouse models. Strikingly, 8866 substantially enhanced the efficacy of docetaxel chemotherapy, resulting in rapid regression of MYC-overexpressing tumors. Collectively, these data establish the synthetic lethal interaction of the IRE1/XBP1 pathway with MYC hyperactivation and provide a potential therapy for MYC-driven human breast cancers.The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that oncogenic MYC regulates the inositol-requiring enzyme 1 (IRE1)/X-box binding protein 1 (XBP1) branch of the UPR in breast cancer via multiple mechanisms. We found that MYC directly controls IRE1 transcription by binding to its promoter and enhancer. Furthermore, MYC forms a transcriptional complex with XBP1, a target of IRE1, and enhances its transcriptional activity. Importantly, we demonstrate that XBP1 is a synthetic lethal partner of MYC. Silencing of XBP1 selectively blocked the growth of MYC-hyperactivated cells. Pharmacological inhibition of IRE1 RNase activity with small molecule inhibitor 8866 selectively restrained the MYC-overexpressing tumor growth in vivo in a cohort of preclinical patient-derived xenograft models and genetically engineered mouse models. Strikingly, 8866 substantially enhanced the efficacy of docetaxel chemotherapy, resulting in rapid regression of MYC-overexpressing tumors. Collectively, these data establish the synthetic lethal interaction of the IRE1/XBP1 pathway with MYC hyperactivation and provide a potential therapy for MYC-driven human breast cancers.
The unfolded protein response (UPR) is a cellular homeostatic mechanism that is activated in many human cancers and plays pivotal roles in tumor progression and therapy resistance. However, the molecular mechanisms for UPR activation and regulation in cancer cells remain elusive. Here, we show that oncogenic MYC regulates the inositol-requiring enzyme 1 (IRE1)/X-box binding protein 1 (XBP1) branch of the UPR in breast cancer via multiple mechanisms. We found that MYC directly controls IRE1 transcription by binding to its promoter and enhancer. Furthermore, MYC forms a transcriptional complex with XBP1, a target of IRE1, and enhances its transcriptional activity. Importantly, we demonstrate that XBP1 is a synthetic lethal partner of MYC. Silencing of XBP1 selectively blocked the growth of MYC-hyperactivated cells. Pharmacological inhibition of IRE1 RNase activity with small molecule inhibitor 8866 selectively restrained the MYC-overexpressing tumor growth in vivo in a cohort of preclinical patient-derived xenograft models and genetically engineered mouse models. Strikingly, 8866 substantially enhanced the efficacy of docetaxel chemotherapy, resulting in rapid regression of MYC-overexpressing tumors. Collectively, these data establish the synthetic lethal interaction of the IRE1/XBP1 pathway with MYC hyperactivation and provide a potential therapy for MYC-driven human breast cancers.
Audience Academic
Author Han, Leng
Chen, Xi
Bu, Wen
Xiang, Yu
Rosen, Jeffrey M.
Dobrolecki, Lacey E.
Lin, Xia
Hu, Dorothy Z.
Shen, Haifa
Lewis, Michael T.
Sun, Zheng
Patterson, John B.
Li, Mingzhou
Yuan, Bo
Feng, Xin-Hua
Kaipparettu, Benny Abraham
Wang, Xiaoran
Li, Feng
Zeng, Qingping
Lu, Yang
Ying, Haoqiang
Zhao, Na
Talukdar, Manisha
Jiang, Yi
Putluri, Nagireddy
Shi, Qing
Liu, Xia
Sicheri, Frank
Wang, Yunfei
Hartig, Sean M.
Xu, Longyong
Chen, Yiwen
Gong, Yingyun
Cao, Jin
Tang, Qianzi
Lv, Xiangdong
AuthorAffiliation 4 Institute of Animal Genetics and Breeding, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, China
3 Dan L. Duncan Cancer Center, Baylor College of Medicine, Houston, Texas, USA
12 Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas, USA
18 Department of Biochemistry, University of Toronto, Toronto, Ontario, Canada
10 Division of Biochemical Genetics, Baylor Genetics, Houston, Texas, USA
2 Lester and Sue Smith Breast Center, and
6 Department of Molecular Genetics, University of Toronto, Toronto, Ontario, Canada
8 Department of Biochemistry and Molecular Biology, The University of Texas Health Science Center at Houston McGovern Medical School, Houston, Texas, USA
16 Fosun Orinove PharmaTech Inc., Suzhou, Jiangsu, China
13 Life Sciences Institute and Innovation Center for Cell Signaling Network, Zhejiang University, Hangzhou, Zhejiang, China
5 Lunenfeld-Tanenbaum Research Institute, Sinai Health System
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29480818$$D View this record in MEDLINE/PubMed
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SubjectTerms Activating transcription factor 1
Animal models
Animals
Biomedical research
Breast cancer
Breast Neoplasms - drug therapy
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer therapies
Cancer treatment
Care and treatment
Cell Line, Tumor
Chemotherapy
Development and progression
Docetaxel - pharmacology
Drug Delivery Systems
Endoplasmic reticulum
Endoribonucleases - genetics
Endoribonucleases - metabolism
Enzymes
Female
Genes
Genetic aspects
Genetic engineering
Health aspects
Humans
Inositol
Kinases
Mice
Molecular modelling
Myc protein
Nucleotidases
Pharmacological research
Phosphorylation
Physiological aspects
Protein folding
Protein-Serine-Threonine Kinases - genetics
Protein-Serine-Threonine Kinases - metabolism
Proteins
Proto-Oncogene Proteins c-myc - genetics
Proto-Oncogene Proteins c-myc - metabolism
Response Elements
Ribonuclease
Saccharomyces cerevisiae
Signal Transduction - drug effects
Signal Transduction - genetics
Stem cells
Transcription
Transcription factors
Tumors
Unfolded Protein Response - drug effects
Unfolded Protein Response - genetics
X-Box Binding Protein 1 - genetics
X-Box Binding Protein 1 - metabolism
Xenograft Model Antitumor Assays
Xenografts
Title Pharmacological targeting of MYC-regulated IRE1/XBP1 pathway suppresses MYC-driven breast cancer
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