Cyr61 promotes breast tumorigenesis and cancer progression

Tsai, Miaw-Sheue; Bogart, Daphne F; Castañeda, Jessica M; Li, Patricia; Lupu, Ruth

doi:10.1038/sj.onc.1205682

Cited by 189Connective Tissue Growth Factor ResearchEstrogen and related hormone effectsAngiogenesis and VEGF in Cancer

Cyr61 promotes breast tumorigenesis and cancer progression

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Tsai, Miaw-Sheue, Bogart, Daphne F, Castañeda, Jessica M, Li, Patricia, Lupu, Ruth·2002·Oncogene

DOI 10.1038/sj.onc.1205682

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Abstract

Cyr61, a member of the CCN family of genes, is an angiogenic factor. We have shown that it is overexpressed in invasive and metastatic human breast cancer cells and tissues. Here, we investigated whether Cyr61 is necessary and/or sufficient to bypass the 'normal' estrogen (E2) requirements for breast cancer cell growth. Our results demonstrate that Cyr61 is sufficient to induce MCF-7 cells to grow in the absence of E2. Cyr61-transfected MCF-7 cells (MCF-7/Cyr61) became E2-independent but still E2-responsive. On the other hand, MCF-7 cells transfected with the vector DNA (MCF-7/V) remain E2-dependent. MCF-7/Cyr61 cells acquire an antiestrogen-resistant phenotype, one of the most common clinical occurrences during breast cancer progression. MCF-7/Cyr61 cells are anchorage-independent and capable of forming Matrigel outgrowth patterns in the absence of E2. ER alpha expression in MCF-7/Cyr61 cells is decreased although still functional. Moreover, MCF-7/Cyr61 cells are tumorigenic in ovariectomized athymic nude mice. The tumors resemble human invasive carcinomas with increased vascularization and overexpression of vascular endothelial growth factor (VEGF). Our results demonstrate that Cyr61 is a tumor-promoting factor and a key regulator of breast cancer progression. This study provides evidence that Cyr61 is sufficient to induce E2-independence and antiestrogen-resistance, and to promote invasiveness in vitro, and to induce tumorigenesis in vivo, all of which are characteristics of an aggressive breast cancer phenotype.

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In MCF7 breast cancer cells, overexpression of CCN1 confers significant resistance to apoptosis, in part through upregulation of XIAP.
“In MCF7 breast cancer cells, which are dependent on estrogen for growth, overexpression of CCN1 renders these cells estrogen-independent and significantly resistant to apoptosis, in part through upregulation of the anti-apoptotic protein XIAP [81,152,153].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [152]
In MCF7 breast cancer cells, overexpression of CCN1 renders the cells estrogen-independent.
“In MCF7 breast cancer cells, which are dependent on estrogen for growth, overexpression of CCN1 renders these cells estrogen-independent and significantly resistant to apoptosis, in part through upregulation of the anti-apoptotic protein XIAP [81,152,153].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [152]

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Authors: Tsai, M.-S., Bogart, D. F., Castañeda, J. M., Li, P., & Lupu, R.
Affiliations: Lawrence Berkeley National Laboratory (US)
Northwestern University (US)
Corresponding author: Lupu, Ruth
ORCID: Tsai, Miaw-Sheue
Lupu, Ruth
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2002-11-19
Volume: 21
Issue: 53
Pages: 8178-8185
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1205682
OpenAlex: W2049976919
Cited by: 189
References: 31
Citations by year: 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 9 · 2020: 9 · 2019: 9 · 2018: 3 · 2017: 4 · 2016: 7 · 2015: 7 · 2014: 10 · 2013: 11 · 2012: 9
FWCI: 4.16
Type: journal article
Language: en
Open access: green
www.osti.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
University of North Texas Digital Library (University of North Texas) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (7r01dk049049-09)
National Institute of Diabetes and Digestive and Kidney Diseases (DK 49049)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connective Tissue Growth Factor Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: CYR61, CCN family, breast cancer progression, antiestrogen resistance, estrogen receptor alpha, tumor angiogenesis, vascular endothelial growth factor, tumor invasion, metastasis, MCF-7 cells, carcinogenesis
MeSH terms: Fulvestrant, Adenocarcinoma, Breast Neoplasms, Collagen, Drug Combinations, Estradiol, Estrogens, Female, Humans, Laminin, Lymphokines, Neoplasm Invasiveness, Neoplasm Proteins, Neoplasms, Hormone-Dependent, Proteoglycans, Receptors, Estrogen, Recombinant Fusion Proteins, Tumor Cells, Cultured, Down-Regulation, Gene Expression Regulation, Neoplastic, Endothelial Growth Factors, Immediate-Early Proteins, Disease Progression, Drug Resistance, Neoplasm, Estrogen Receptor Modulators, Intercellular Signaling Peptides and Proteins, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A, Estrogen Receptor alpha, Cysteine-Rich Protein 61

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Cyr61 promotes breast tumorigenesis and cancer progression

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