EZH2 Promotes Expansion of Breast Tumor Initiating Cells through Activation of RAF1-β-Catenin Signaling

It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been li...

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Published in	Cancer cell Vol. 19; no. 1; pp. 86 - 100
Main Authors	Chang, Chun-Ju, Yang, Jer-Yen, Xia, Weiya, Chen, Chun-Te, Xie, Xiaoming, Chao, Chi-Hong, Woodward, Wendy A., Hsu, Jung-Mao, Hortobagyi, Gabriel N., Hung, Mien-Chie
Format	Journal Article
Language	English
Published	United States Elsevier Inc 18.01.2011
Subjects	Animals Benzenesulfonates - pharmacology Benzimidazoles - pharmacology Benzimidazoles - therapeutic use beta Catenin - metabolism Breast Neoplasms - diagnosis Breast Neoplasms - drug therapy Breast Neoplasms - metabolism Breast Neoplasms - pathology Cell Hypoxia - physiology Cell Line, Tumor Cell Proliferation - drug effects Cell Survival - drug effects Cell Survival - physiology Centrosome - pathology Chromosome Aberrations DNA Breaks, Double-Stranded DNA Damage - genetics DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Enhancer of Zeste Homolog 2 Protein Extracellular Signal-Regulated MAP Kinases - metabolism Female Gene Expression - drug effects Gene Expression - genetics Gene Expression Regulation, Neoplastic - physiology Humans Mice Mice, Inbred NOD Mice, SCID Models, Biological Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Niacinamide - analogs & derivatives Phenylurea Compounds Phosphorylation - drug effects Polycomb Repressive Complex 2 Proto-Oncogene Proteins c-raf - genetics Proto-Oncogene Proteins c-raf - metabolism Pyridines - pharmacology Rad51 Recombinase - genetics Rad51 Recombinase - metabolism Signal Transduction - drug effects Signal Transduction - physiology Sorafenib Spheroids, Cellular - drug effects Spheroids, Cellular - pathology Transcription Factors - genetics Transcription Factors - metabolism Transplantation, Heterologous - pathology Xenograft Model Antitumor Assays
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Abstract	It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs. ► Increased EZH2 expression in BTICs enhances BTIC survival and proliferation ► EZH2-amplified RAF1-β-catenin signaling promotes BTIC expansion ► Hypoxic microenvironment promotes BTICs through upregulating EZH2 expression ► AZD6244 suppresses BTICs by inhibiting activated RAF1-ERK-β-catenin signaling
AbstractList	It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs. ► Increased EZH2 expression in BTICs enhances BTIC survival and proliferation ► EZH2-amplified RAF1-β-catenin signaling promotes BTIC expansion ► Hypoxic microenvironment promotes BTICs through upregulating EZH2 expression ► AZD6244 suppresses BTICs by inhibiting activated RAF1-ERK-β-catenin signaling It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs. It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs.It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs. It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK- beta -catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs. a-[ordm Increased EZH2 expression in BTICs enhances BTIC survival and proliferation a-[ordm EZH2-amplified RAF1- beta -catenin signaling promotes BTIC expansion a-[ordm Hypoxic microenvironment promotes BTICs through upregulating EZH2 expression a-[ordm AZD6244 suppresses BTICs by inhibiting activated RAF1-ERK- beta -catenin signaling It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of additional genetic mutations and drives cancer progression. Overexpression of Polycomb protein EZH2, essential in stem cell self-renewal, has been linked to breast cancer progression. However, critical mechanism linking increased EZH2 expression to BTIC (breast tumor initiating cell) regulation and cancer progression remains unclear. Here, we identify a mechanism in which EZH2 expression-mediated downregulation of DNA damage repair leads to accumulation of recurrent RAF1 gene amplification in BTICs, which activates p-ERK-β-catenin signaling to promote BTIC expansion. We further reveal that AZD6244, a clinical trial drug that inhibits RAF1-ERK signaling, could prevent breast cancer progression by eliminating BTICs.
Author	Hsu, Jung-Mao Woodward, Wendy A. Hung, Mien-Chie Xia, Weiya Xie, Xiaoming Chen, Chun-Te Chang, Chun-Ju Chao, Chi-Hong Hortobagyi, Gabriel N. Yang, Jer-Yen
AuthorAffiliation	3 Department of Breast Medical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA 1 Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA 6 Asia University, Taichung 413, Taiwan 2 Department of Radiation Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA 5 The Center for Molecular Medicine and Graduate Institute of Cancer Biology, China Medical University and Hospital, Taichung 404, Taiwan
AuthorAffiliation_xml	– name: 3 Department of Breast Medical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – name: 1 Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – name: 6 Asia University, Taichung 413, Taiwan – name: 2 Department of Radiation Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – name: 5 The Center for Molecular Medicine and Graduate Institute of Cancer Biology, China Medical University and Hospital, Taichung 404, Taiwan
Author_xml	– sequence: 1 givenname: Chun-Ju surname: Chang fullname: Chang, Chun-Ju organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 2 givenname: Jer-Yen surname: Yang fullname: Yang, Jer-Yen organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 3 givenname: Weiya surname: Xia fullname: Xia, Weiya organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 4 givenname: Chun-Te surname: Chen fullname: Chen, Chun-Te organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 5 givenname: Xiaoming surname: Xie fullname: Xie, Xiaoming organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 6 givenname: Chi-Hong surname: Chao fullname: Chao, Chi-Hong organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 7 givenname: Wendy A. surname: Woodward fullname: Woodward, Wendy A. organization: Department of Radiation Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 8 givenname: Jung-Mao surname: Hsu fullname: Hsu, Jung-Mao organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 9 givenname: Gabriel N. surname: Hortobagyi fullname: Hortobagyi, Gabriel N. organization: Department of Breast Medical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA – sequence: 10 givenname: Mien-Chie surname: Hung fullname: Hung, Mien-Chie email: mhung@mdanderson.org organization: Department of Molecular and Cellular Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, TX 77030, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21215703$$D View this record in MEDLINE/PubMed
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Snippet	It has been proposed that an aggressive secondary cancer stem cell population arises from a primary cancer stem cell population through acquisition of...
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SubjectTerms	Animals Benzenesulfonates - pharmacology Benzimidazoles - pharmacology Benzimidazoles - therapeutic use beta Catenin - metabolism Breast Neoplasms - diagnosis Breast Neoplasms - drug therapy Breast Neoplasms - metabolism Breast Neoplasms - pathology Cell Hypoxia - physiology Cell Line, Tumor Cell Proliferation - drug effects Cell Survival - drug effects Cell Survival - physiology Centrosome - pathology Chromosome Aberrations DNA Breaks, Double-Stranded DNA Damage - genetics DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Enhancer of Zeste Homolog 2 Protein Extracellular Signal-Regulated MAP Kinases - metabolism Female Gene Expression - drug effects Gene Expression - genetics Gene Expression Regulation, Neoplastic - physiology Humans Mice Mice, Inbred NOD Mice, SCID Models, Biological Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Niacinamide - analogs & derivatives Phenylurea Compounds Phosphorylation - drug effects Polycomb Repressive Complex 2 Proto-Oncogene Proteins c-raf - genetics Proto-Oncogene Proteins c-raf - metabolism Pyridines - pharmacology Rad51 Recombinase - genetics Rad51 Recombinase - metabolism Signal Transduction - drug effects Signal Transduction - physiology Sorafenib Spheroids, Cellular - drug effects Spheroids, Cellular - pathology Transcription Factors - genetics Transcription Factors - metabolism Transplantation, Heterologous - pathology Xenograft Model Antitumor Assays
Title	EZH2 Promotes Expansion of Breast Tumor Initiating Cells through Activation of RAF1-β-Catenin Signaling
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