17β‐estradiol upregulates GREB1 and accelerates ovarian tumor progression in vivo

Exogenous 17β‐estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG‐LS‐TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian t...

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Veröffentlicht in:International journal of cancer Jg. 135; H. 5; S. 1072 - 1084
Hauptverfasser: Laviolette, Laura A., Hodgkinson, Kendra M., Minhas, Neha, Perez‐Iratxeta, Carol, Vanderhyden, Barbara C.
Format: Journal Article
Sprache:Englisch
Veröffentlicht: Hoboken, NJ Wiley-Blackwell 01.09.2014
BlackWell Publishing Ltd
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ISSN:0020-7136, 1097-0215, 1097-0215
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Abstract Exogenous 17β‐estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG‐LS‐TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG‐LS‐TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2‐derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 (Greb1) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference‐mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention. What's new? Post‐menopausal estrogen‐only hormone replacement therapy is associated with an increased risk of epithelial ovarian cancer, the development of which may be influenced by the actions of 17β‐estradiol (E2) on ovarian surface epithelium (OSE). Here, in an orthotopic mouse model of ovarian cancer, E2 was found to accelerate tumor progression. Microarray analysis identified 197 E2‐upregulated and 55 E2‐downregulated genes. Among E2‐upregulated genes was Greb1. GREB1 protein was highly upregulated in human tumors relative to normal human OSE, suggesting that it may be a tumor‐promoting factor and potential mediator of E2‐stimulated tumor growth.
AbstractList Exogenous 17β‐estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG‐LS‐TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG‐LS‐TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2‐derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 ( Greb1 ) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference‐mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention. What's new? Post‐menopausal estrogen‐only hormone replacement therapy is associated with an increased risk of epithelial ovarian cancer, the development of which may be influenced by the actions of 17β‐estradiol (E2) on ovarian surface epithelium (OSE). Here, in an orthotopic mouse model of ovarian cancer, E2 was found to accelerate tumor progression. Microarray analysis identified 197 E2‐upregulated and 55 E2‐downregulated genes. Among E2‐upregulated genes was Greb1 . GREB1 protein was highly upregulated in human tumors relative to normal human OSE, suggesting that it may be a tumor‐promoting factor and potential mediator of E2‐stimulated tumor growth.
Exogenous 17β-estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG-LS-TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG-LS-TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2-derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 (Greb1) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference-mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention.
Exogenous 17β‐estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG‐LS‐TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG‐LS‐TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2‐derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 (Greb1) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference‐mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention. What's new? Post‐menopausal estrogen‐only hormone replacement therapy is associated with an increased risk of epithelial ovarian cancer, the development of which may be influenced by the actions of 17β‐estradiol (E2) on ovarian surface epithelium (OSE). Here, in an orthotopic mouse model of ovarian cancer, E2 was found to accelerate tumor progression. Microarray analysis identified 197 E2‐upregulated and 55 E2‐downregulated genes. Among E2‐upregulated genes was Greb1. GREB1 protein was highly upregulated in human tumors relative to normal human OSE, suggesting that it may be a tumor‐promoting factor and potential mediator of E2‐stimulated tumor growth.
Exogenous 17β-estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG-LS-TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG-LS-TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2-derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 (Greb1) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference-mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention.Exogenous 17β-estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG-LS-TAg mouse model of the disease. We hypothesized that E2 has direct effects on ovarian cancer cells and this study was designed to determine the molecular mechanisms by which E2 accelerates ovarian tumor progression. Mouse ovarian cancer ascites (MAS) cell lines were derived from tgCAG-LS-TAg mice. Following intraperitoneal engraftment of two MAS cell lines, MASC1 and MASE2, into SCID mice, exogenous E2 significantly decreased the survival time and increased the tumor burden. Microarray analysis performed on MASE2-derived tumors treated with E2 or placebo showed that E2 treatment caused the upregulation of 197 genes and the downregulation of 55 genes. The expression of gene regulated by estrogen in breast cancer 1 (Greb1) was upregulated in mouse tumors treated with E2 and was overexpressed in human ovarian cancers relative to human ovarian surface epithelium, suggesting a role for GREB1 in human ovarian tumor progression. RNA interference-mediated knockdown of GREB1 in MASE2 cells decreased their proliferation rate in vitro and increased survival time in mice engrafted with the cells. These results emphasize the importance of E2 in ovarian tumor progression and identify Greb1 as a novel gene target for therapeutic intervention.
Author Perez‐Iratxeta, Carol
Hodgkinson, Kendra M.
Laviolette, Laura A.
Vanderhyden, Barbara C.
Minhas, Neha
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  surname: Hodgkinson
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  organization: Centre for Cancer Therapeutics, Ottawa Hospital Research Institute
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  organization: Centre for Cancer Therapeutics, Ottawa Hospital Research Institute
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  surname: Perez‐Iratxeta
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  givenname: Barbara C.
  surname: Vanderhyden
  fullname: Vanderhyden, Barbara C.
  organization: University of Ottawa
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IsDoiOpenAccess true
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Issue 5
Keywords Animal model
mouse model
ovarian cancer
Ovary cancer
Rodentia
Estrogen
GREB1
17β-Estradiol
Malignant tumor
Ovarian hormone
Female genital diseases
Ovarian diseases
In vivo
Vertebrata
microarray
Mammalia
Cancerology
Mouse
Tumor progression
Sex steroid hormone
Cancer
Ovarian tumor
estrogen
Language English
License Attribution-NonCommercial-NoDerivs
http://creativecommons.org/licenses/by-nc-nd/3.0
CC BY 4.0
2014 The Authors. Published by Wiley Periodicals, Inc. on behalf of UICC.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
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Notes L.A.L and K.M.H. contributed equally to this work
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Grant sponsor: Ovarian Cancer Canada for its financial support of the Ottawa Ovarian Cancer Tissue Bank, Canadian Institutes of Health Research (B.C.V.), a doctoral research award from the Canadian Institutes of Health Research-Ontario Women’s Health Council/Institute of Gender and Health (L.A.L.), a Frederick Banting and Charles Best Canada Graduate Scholarship Master’s Award (K.M.H.), an Ontario Graduate Scholarship (K.M.H.), a doctoral research award from the CIHR Training Program in Reproduction, Early Development and the Impact on Health (K.M.H.), Teal Heart award from Ovarian Cancer Canada (K.M.H.)
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Snippet Exogenous 17β‐estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG‐LS‐TAg mouse model of the disease. We hypothesized that E2...
Exogenous 17β-estradiol (E2) accelerates the progression of ovarian cancer in the transgenic tgCAG-LS-TAg mouse model of the disease. We hypothesized that E2...
SourceID pubmedcentral
proquest
pubmed
pascalfrancis
crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 1072
SubjectTerms Animals
Biological and medical sciences
Cancer Genetics
Carcinoma, Ovarian Epithelial
Cell Line, Tumor
Cell Proliferation
Disease Progression
Down-Regulation
Estradiol - pharmacology
estrogen
Female
Female genital diseases
Gene Expression Regulation, Neoplastic - drug effects
GREB1
Gynecology. Andrology. Obstetrics
Humans
Medical sciences
Mice
Mice, SCID
microarray
mouse model
Multiple tumors. Solid tumors. Tumors in childhood (general aspects)
Neoplasm Proteins - biosynthesis
Neoplasm Proteins - genetics
Neoplasms, Glandular and Epithelial - genetics
Neoplasms, Glandular and Epithelial - pathology
ovarian cancer
Ovarian Neoplasms - genetics
Ovarian Neoplasms - pathology
RNA Interference
RNA, Small Interfering - genetics
Tumor Burden - drug effects
Tumors
Up-Regulation
Title 17β‐estradiol upregulates GREB1 and accelerates ovarian tumor progression in vivo
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fijc.28741
https://www.ncbi.nlm.nih.gov/pubmed/24469735
https://www.proquest.com/docview/1536684809
https://pubmed.ncbi.nlm.nih.gov/PMC4235304
Volume 135
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