Genomic and phenotypic analysis reveals a key role for CCN1 (CYR61) in BAG3—modulated adhesion and invasion
Open accessAbstract
Chaperone protein quantity may regulate the balance of proteins involved in invasion and malignancy. BAG3 is a co‐chaperone and pro‐survival protein that has been implicated in adhesion, migration, and metastasis. We reported that BAG3 overexpression in MDA435 human breast cancer cells results in a significant decrease in migration and adhesion to matrix molecules that is reversed upon deletion of the BAG3 proline‐rich domain (dPXXP). We now hypothesize that transcriptional analysis would identify proteins involved in matrix‐related processes that are regulated by BAG3 and/or its PXXP domain mutant. Expression array analysis of MDA435 cells overexpressing either wild‐type BAG3 (FL) or dPXXP identified CCN1 as a BAG3 target protein. CCN1 is a known AP‐1 target. Increased AP‐1 transcriptional activity and AP‐1 DNA‐binding was found in MDA435 dPXXP cells. Consistent with these findings, CCN1 quantity and secretion were increased in dPXXP mutants but suppressed in FL cells; both BAG3 forms resulted in up‐regulated CCN1 in HeLa cells. CCN1 silencing in the BAG3 FL overexpressors reduced the already low phospho‐integrin β1 in response to attachment on collagen IV. Matrigel invasion of HeLa cells engineered with the BAG3 constructs was enhanced in FL cells and minimal in dPXXP cells. CCN1 silencing blocked a greater percentage of the serum‐induced invasion in FL cells than in dPXXP cells. This implies a context‐dependent function of BAG3 on CCN1 and thus mesenchymal behaviour. CCN1 may be necessary for adhesion and matrix‐related signalling in FL cells, abrogating a negative signal of the PXXP domain when BAG3 is intact. We propose that BAG3 regulates CCN1 expression to regulate tumour cell adhesion and migration. Published in 2009 by John Wiley & Sons, Ltd.
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CCN1 stimulates cell migration in fibroblasts, smooth muscle cells, endothelial cells, and certain cancer cells.
“Furthermore, CCN1 stimulates cell migration in fibroblasts, smooth muscle cells and endothelial cells [56,71,72], and certain cancer cells [73–75].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [75]
CCN1 can promote cancer cell proliferation, invasion, survival, and metastasis.
“In addition to angiogenesis, CCN1 can also promote cancer cell proliferation, invasion, survival, and metastasis [74,75,141].”
From CCN1/CYR61: the very model of a modern matricellular protein (2011) · cites this paper as [75]
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- Authors
- Kassis, J. N., Virador, V. M., Guancial, E. A., Kimm, D., Ho, A. S., Mishra, M., Chuang, E. Y., Cook, J., Gius, D., & Kohn, E. C.
- Affiliations
- National Cancer Institute (US)
- Corresponding author
- Kohn, Elise C
- ORCID
- Venue
- The Journal of Pathology
- Publisher
- Wiley
- Published
- 2009-04-28
- Volume
- 218
- Issue
- 4
- Pages
- 495-504
- ISSN
- 0022-3417 (ISSN-L)
- 1096-9896
- PMC
- PMC7316387
- OpenAlex
- W1972926205
- Cited by
- 34
- References
- 40
- Citations by year
- 2026: 1 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 5 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 2 · 2015: 5 · 2014: 1 · 2013: 3 · 2012: 1
- FWCI
- 0.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Pathology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, public-domain)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (1z01bc010443-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connective Tissue Growth Factor Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Health Sciences › Medicine › Rheumatology › Bone and Dental Protein Studies
- Keywords
- BAG3, CYR61, molecular chaperones, breast cancer, cell adhesion, cell invasion, cell-matrix adhesion, AP-1 transcription, tumor cell migration, MDA-MB-435 cells, HeLa cells, gene silencing
- MeSH terms
- Cell Adhesion, Collagen, Drug Combinations, HeLa Cells, Humans, Laminin, Neoplasm Invasiveness, Phosphorylation, Proteoglycans, RNA, Messenger, Up-Regulation, Integrin beta1, Oligonucleotide Array Sequence Analysis, Gene Silencing, Gene Expression Profiling, Genomics, Electrophoretic Mobility Shift Assay, Cell Line, Tumor, Adaptor Proteins, Signal Transducing, Apoptosis Regulatory Proteins, Cysteine-Rich Protein 61
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