CDK2-mediated site-specific phosphorylation of EZH2 drives and maintains triple-negative breast cancer

Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphor...

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Published inNature communications Vol. 10; no. 1; pp. 5114 - 15
Main Authors Nie, Lei, Wei, Yongkun, Zhang, Fei, Hsu, Yi-Hsin, Chan, Li-Chuan, Xia, Weiya, Ke, Baozhen, Zhu, Cihui, Deng, Rong, Tang, Jun, Yao, Jun, Chu, Yu-Yi, Zhao, Xixi, Han, Ye, Hou, Junwei, Huo, Longfei, Ko, How-Wen, Lin, Wan-Chi, Yamaguchi, Hirohito, Hsu, Jung-Mao, Yang, Yi, Pan, Dean N., Hsu, Jennifer L., Kleer, Celina G., Davidson, Nancy E., Hortobagyi, Gabriel N., Hung, Mien-Chie
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.11.2019
Nature Publishing Group
Nature Portfolio
Subjects
13/1
13/106
13/51
38/91
631/67/1059
631/67/1059/602
631/67/1347
Animals
Benzamides - pharmacology
Breast cancer
Bridged Bicyclo Compounds, Heterocyclic - pharmacology
Cyclin E
Cyclin-dependent kinase 2
Cyclin-Dependent Kinase 2 - antagonists & inhibitors
Cyclin-Dependent Kinase 2 - metabolism
Cyclin-dependent kinases
Enhancer of Zeste Homolog 2 Protein - antagonists & inhibitors
Enhancer of Zeste Homolog 2 Protein - genetics
Enhancer of Zeste Homolog 2 Protein - metabolism
Epidermal growth factor
ErbB-2 protein
Estrogen Receptor alpha - drug effects
Estrogen Receptor alpha - genetics
Estrogen Receptor alpha - metabolism
Estrogens
Female
Growth factors
Homology
Humanities and Social Sciences
Humans
Kinases
Mammary gland
Mammary glands
Mammary Glands, Human - drug effects
Mammary Glands, Human - metabolism
Mammary Neoplasms, Experimental - genetics
Mammary Neoplasms, Experimental - metabolism
Mice
Mice, Transgenic
Mimicry
multidisciplinary
Phenotypes
Phosphorylation
Progesterone
Pyridinium Compounds - pharmacology
Pyridones - pharmacology
Receptor, ErbB-2 - genetics
Receptor, ErbB-2 - metabolism
Receptors, Progesterone - metabolism
Science
Science (multidisciplinary)
Tamoxifen
Transgenic mice
Triple Negative Breast Neoplasms - genetics
Triple Negative Breast Neoplasms - metabolism
Tumors
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-019-13105-5

Cover

Abstract Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2 T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2 T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC. EZH2 phosphorylation by CDK2 promotes progression of triple-negative breast cancer (TNBC). Here, the authors show that this signaling axis downregulates ERα, and thus combinatorial blockade of CDK2 and EZH2 sensitizes TNBC cells to tamoxifen.
AbstractList EZH2 phosphorylation by CDK2 promotes progression of triple-negative breast cancer (TNBC). Here, the authors show that this signaling axis downregulates ERα, and thus combinatorial blockade of CDK2 and EZH2 sensitizes TNBC cells to tamoxifen.
Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2 T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2 T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC.
Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC.EZH2 phosphorylation by CDK2 promotes progression of triple-negative breast cancer (TNBC). Here, the authors show that this signaling axis downregulates ERα, and thus combinatorial blockade of CDK2 and EZH2 sensitizes TNBC cells to tamoxifen.
Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2 T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2 T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC. EZH2 phosphorylation by CDK2 promotes progression of triple-negative breast cancer (TNBC). Here, the authors show that this signaling axis downregulates ERα, and thus combinatorial blockade of CDK2 and EZH2 sensitizes TNBC cells to tamoxifen.
Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2 in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2 in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC.
Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC.Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2) expression, is closely related to basal-like breast cancer. Previously, we and others report that cyclin E/cyclin-dependent kinase 2 (CDK2) phosphorylates enhancer of zeste homolog 2 (EZH2) at T416 (pT416-EZH2). Here, we show that transgenic expression of phospho-mimicking EZH2 mutant EZH2T416D in mammary glands leads to tumors with TNBC phenotype. Coexpression of EZH2T416D in mammary epithelia of HER2/Neu transgenic mice reprograms HER2-driven luminal tumors into basal-like tumors. Pharmacological inhibition of CDK2 or EZH2 allows re-expression of ERα and converts TNBC to luminal ERα-positive, rendering TNBC cells targetable by tamoxifen. Furthermore, the combination of either CDK2 or EZH2 inhibitor with tamoxifen effectively suppresses tumor growth and markedly improves the survival of the mice bearing TNBC tumors, suggesting that the mechanism-based combination therapy may be an alternative approach to treat TNBC.
ArticleNumber 5114
Author Ke, Baozhen
Deng, Rong
Hung, Mien-Chie
Chan, Li-Chuan
Pan, Dean N.
Nie, Lei
Davidson, Nancy E.
Hortobagyi, Gabriel N.
Hsu, Jung-Mao
Xia, Weiya
Tang, Jun
Lin, Wan-Chi
Yamaguchi, Hirohito
Yao, Jun
Chu, Yu-Yi
Ko, How-Wen
Huo, Longfei
Zhu, Cihui
Hou, Junwei
Hsu, Yi-Hsin
Kleer, Celina G.
Wei, Yongkun
Hsu, Jennifer L.
Zhao, Xixi
Zhang, Fei
Han, Ye
Yang, Yi
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  fullname: Wei, Yongkun
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  givenname: Fei
  surname: Zhang
  fullname: Zhang, Fei
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Department of General Surgery, Xinhua Hospital affiliated to Shanghai Jiao Tong University School of Medicine
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Graduate School of Biomedical Sciences, The University of Texas Health Science Center at Houston
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, State Key Laboratory of Oncology in South China, Cancer Center, Sun Yat-Sen University
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Department of Breast Oncology, Cancer Center, Sun Yat-Sen University
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  givenname: Hirohito
  surname: Yamaguchi
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Cancer Research Center, Qatar Biomedical Research Institute, Hamad Bin Khalifa University, Qatar Foundation
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  givenname: Jung-Mao
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31704972$$D View this record in MEDLINE/PubMed
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– reference: 31996688 - Nat Commun. 2020 Jan 29;11(1):673
SSID ssj0000391844
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Snippet Triple-negative breast cancer (TNBC), which lacks estrogen receptor α (ERα), progesterone receptor, and human epidermal growth factor receptor 2 (HER2)...
EZH2 phosphorylation by CDK2 promotes progression of triple-negative breast cancer (TNBC). Here, the authors show that this signaling axis downregulates ERα,...
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proquest
pubmed
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StartPage 5114
SubjectTerms 13/1
13/106
13/51
38/91
631/67/1059
631/67/1059/602
631/67/1347
Animals
Benzamides - pharmacology
Breast cancer
Bridged Bicyclo Compounds, Heterocyclic - pharmacology
Cyclin E
Cyclin-dependent kinase 2
Cyclin-Dependent Kinase 2 - antagonists & inhibitors
Cyclin-Dependent Kinase 2 - metabolism
Cyclin-dependent kinases
Enhancer of Zeste Homolog 2 Protein - antagonists & inhibitors
Enhancer of Zeste Homolog 2 Protein - genetics
Enhancer of Zeste Homolog 2 Protein - metabolism
Epidermal growth factor
ErbB-2 protein
Estrogen Receptor alpha - drug effects
Estrogen Receptor alpha - genetics
Estrogen Receptor alpha - metabolism
Estrogens
Female
Growth factors
Homology
Humanities and Social Sciences
Humans
Kinases
Mammary gland
Mammary glands
Mammary Glands, Human - drug effects
Mammary Glands, Human - metabolism
Mammary Neoplasms, Experimental - genetics
Mammary Neoplasms, Experimental - metabolism
Mice
Mice, Transgenic
Mimicry
multidisciplinary
Phenotypes
Phosphorylation
Progesterone
Pyridinium Compounds - pharmacology
Pyridones - pharmacology
Receptor, ErbB-2 - genetics
Receptor, ErbB-2 - metabolism
Receptors, Progesterone - metabolism
Science
Science (multidisciplinary)
Tamoxifen
Transgenic mice
Triple Negative Breast Neoplasms - genetics
Triple Negative Breast Neoplasms - metabolism
Tumors
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Title CDK2-mediated site-specific phosphorylation of EZH2 drives and maintains triple-negative breast cancer
URI https://link.springer.com/article/10.1038/s41467-019-13105-5
https://www.ncbi.nlm.nih.gov/pubmed/31704972
https://www.proquest.com/docview/2313069261
https://www.proquest.com/docview/2313381132
https://pubmed.ncbi.nlm.nih.gov/PMC6841924
https://doaj.org/article/db070b7abc844972aa2cc8c48facb949
Volume 10
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