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BMC Cancer
Published in: BMC Cancer 1/2024

Open Access 01-12-2024 | Breast Cancer | Research

Dual effect of vitamin D3 on breast cancer-associated fibroblasts

Authors: Natalia Łabędź, Artur Anisiewicz, Martyna Stachowicz-Suhs, Joanna Banach, Dagmara Kłopotowska, Adam Maciejczyk, Patrycja Gazińska, Aleksandra Piotrowska, Piotr Dzięgiel, Rafał Matkowski, Joanna Wietrzyk

Published in: BMC Cancer | Issue 1/2024

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Abstract

Background

Cancer-associated fibroblasts (CAFs) play an important role in the tumor microenvironment. Despite the well-known in vitro antitumoral effect of vitamin D3 (VD3), its impact on breast CAFs is almost unknown. In this study, we analyzed the ex vivo effects of calcitriol on CAFs isolated from breast cancer tissues.

Methods

CAFs were cultured with 1 and 10 nM calcitriol and their phenotype; gene expression, protein expression, and secretion were assessed. Calcitriol-treated CAFs-conditioned media (CM) were used to analyze the effect of CAFs on the migration and protein expression of MCF-7 and MDA-MB-231 cells.

Results

Tumor tissues from VD3-deficient patients exhibited lower levels of β-catenin and TGFβ1, along with higher levels of CYP24A1 compared to VD3-normal patients. In VD3-deficient patients, CAF infiltration was inversely associated with CYP24A1 levels and positively correlated with OPN levels. Calcitriol diminished CAFs’ viability, but this effect was weaker in premenopausal and VD3-normal patients. Calcitriol reduced mRNA expression of CCL2, MMP9, TNC, and increased PDPN, SPP1, and TIMP1. It also decreased the secretion of CCL2, TNC, and the activity of MMP-2, while increasing cellular levels of TIMP1 in CAFs from all patient groups. In nonmetastatic and postmenopausal patients, PDPN surface expression increased, and CAFs CM from these groups decreased MCF-7 cell migration after ex vivo calcitriol treatment. In premenopausal and VD3-deficient patients, calcitriol reduced IDO1 expression in CAFs. Calcitriol-treated CAFs CM from these patients decreased OPN expression in MCF-7 and/or MDA-MB-231 cells. However, in premenopausal patients, calcitriol-treated CAFs CM also decreased E-cadherin expression in both cell lines.

Conclusion

The effects of calcitriol on breast CAFs, both at the gene and protein levels, are complex, reflecting the immunosuppressive or procancer properties of CAFs. The anticancer polarization of CAFs following ex vivo calcitriol treatment may result from decreased CCL2, TNC (gene and protein), MMP9, and MMP-2, while the opposite effect may result from increased PDPN, TIMP1 (gene and protein), and SPP1. Despite these multifaceted effects of calcitriol on molecule expression, CAFs’ CMs from nonmetastatic and postmenopausal patients treated ex vivo with calcitriol decreased the migration of MCF-7 cells.
Appendix
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Metadata
Title
Dual effect of vitamin D3 on breast cancer-associated fibroblasts
Authors
Natalia Łabędź
Artur Anisiewicz
Martyna Stachowicz-Suhs
Joanna Banach
Dagmara Kłopotowska
Adam Maciejczyk
Patrycja Gazińska
Aleksandra Piotrowska
Piotr Dzięgiel
Rafał Matkowski
Joanna Wietrzyk
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2024
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-024-11961-z

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