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Exosomes released by oxidative stress-induced mesenchymal stem cells promote murine mammary tumor progression through activating the STAT3 signaling pathway

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Abstract

Mesenchymal stem cells (MSCs) may play a pivotal role in shaping the tumor microenvironment (TME), influencing tumor growth. Nonetheless, conflicting evidence exists regarding the distinct impacts of MSCs on tumor progression, with some studies suggesting promotion while others indicate suppression of tumor cell growth. Considering that oxidative stress is implicated in the dynamic interaction between components of the TME and tumor cells, we investigated the contribution of exosomes released by hydrogen peroxide (H2O2)-treated MSCs to murine mammary tumor growth and progression. Additionally, we aimed to identify the underlying mechanism through which MSC-derived exosomes affect breast tumor growth and angiogenesis. Our findings demonstrated that exosomes released by H2O2-treated, stress-induced MSCs (St-MSC Exo) promoted breast cancer cell progression by inducing the expression of vascular endothelial growth factor (VEGF) and markers associated with epithelial-to-mesenchymal transition. Further clarification revealed that the promoting effect of St-MSC Exo on VEGF expression may, in part, depend on activating STAT3 signaling in BC cells. In contrast, exosomes derived from untreated MSCs retarded JAK1/STAT3 phosphorylation and reduced VEGF expression. Additionally, our observations revealed that the activation of the transcription factor NF-κB in BC cells, stimulated with St-MSC Exo, occurs concurrently with an increase in intracellular ROS production. Moreover, we observed that the increase in VEGF secretion into the conditioned media of 4T1 BC, mediated by St-MSC Exo, positively influenced endothelial cell proliferation, migration, and vascular behavior in vitro. In turn, our in vivo studies confirmed that St-MSC Exo, but not exosomes derived from untreated MSCs, exhibited a significant promoting effect on breast tumorigenicity. Collectively, our findings provide new insights into how MSCs may contribute to modulating the TME. We propose a novel mechanism through which exosomes derived from oxidative stress-induced MSCs may contribute to tumor progression and angiogenesis.

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Data Availability

The data supporting the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

The authors are grateful to the members of the Department of Molecular Genetics at Tarbiat Modares University for their excellent support. This work was supported financially by Tarbiat Modares University.

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This work was supported financially by Tarbiat Modares University.

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Authors and Affiliations

  1. Department of Molecular Genetics, Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran

    Mansour Almouh, Katayoon Pakravan, Mohammad H. Ghazimoradi, Romina Motamed, Babak Bakhshinejad & Sadegh Babashah

  2. Department of Immunology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

    Zuhair Mohammad Hassan

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  1. Mansour Almouh
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Contributions

S.B. conceived and designed the study. M.A., K.P., and M.G. performed all the experiments. Z.M.H and M.G. contributed to the provision of study materials. M.A. drafted the manuscript, and B.B., R.M., and S.B. contributed to revising it. S.B. supervised the study and provided administrative support. All the authors reviewed and approved the final manuscript.

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Correspondence to Sadegh Babashah.

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Almouh, M., Pakravan, K., Ghazimoradi, M.H. et al. Exosomes released by oxidative stress-induced mesenchymal stem cells promote murine mammary tumor progression through activating the STAT3 signaling pathway. Mol Cell Biochem (2024). https://doi.org/10.1007/s11010-024-04934-0

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