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Mitochondrial transfer in PC-3 cells fingerprinted in ferroptosis sensitivity: a brand new approach targeting cancer metabolism

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Abstract

Despite recent therapeutic advancements, cancer remains one of the leading causes of death worldwide, with mitochondrial dysfunction being associated with cancer initiation and progression, along with chemotherapeutic resistance and ferroptotic cell death failure; however, the significance of mitochondria in various cancer types remains a matter of debate for the moment. The aim of this study is to ascertain the outcome of transferring healthy mitochondria into the aggressive and rapidly proliferating prostate cancer (PC-3) cells and afterwards evaluate the efficacy of combination therapy with or without the ferroptosis inducer erastin. In this sense, normal mitochondria were first isolated from human umbilical cord-derived mesenchymal stem cells, human umbilical vein endothelial cells, and human embryonic kidney cells and were later transferred into PC-3 cells and rhodamine 6G-treated PC-3 cells exhibiting mitochondrial dysfunction. Next, cell proliferation and sensitivity to cisplatin were measured using Cell Counting Kit-8 and the Malondialdehyde Assay Lipid Peroxidation Kit, respectively, along with ferroptotic damage. Transferring the healthy mitochondria into PC-3 cells was observed to increase cell proliferation and rescue the cisplatin-induced cell death, but not the erastin-induced ferroptosis, as in mitochondrial transfer effectively enhanced erastin-mediated ferroptosis in PC-3 cells. Hence, the introduction of healthy mitochondria into the highly aggressive and proliferating cancer cells would be deemed a brand new therapeutic strategy for a variety of cancers.

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Funding

The present study was supported financially by the Research Deputy of Guilan University of Medical Sciences (Grant No: 1400042807) and approved by the Ethics Committee of Guilan University of Medical Sciences (Code number: IR.GUMS.REC.1400.205).

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Authors and Affiliations

  1. Department of Medical Biotechnology, Faculty of Paramedicine, Guilan University of Medical Sciences, Rasht, Iran

    Amirsadegh Nikoo

  2. Burn and Regenerative Medicine Research Center, Velayat Hospital, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Mehryar Habibi Roudkenar, Zahra Pourmohammadi-Bejarpasi & Amaneh Mohammadi Roushandeh

  3. Department of Applied Pharmacology, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima, Japan

    Tomoaki Sato & Kazuo Tomita

  4. Division of Radiation Biology and Medicine, Faculty of Medicine, Tohoku Medical and Pharmaceutical University, Sendai, Japan

    Yoshikazu Kuwahara

  5. Department of Medical Laboratory Sciences, Faculty of Paramedicine, Tabriz University of Medical Sciences, Tabriz, Iran

    Nima Najafi-Ghalehlou

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  1. Amirsadegh Nikoo
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  2. Mehryar Habibi Roudkenar
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Nikoo, A., Roudkenar, M.H., Sato, T. et al. Mitochondrial transfer in PC-3 cells fingerprinted in ferroptosis sensitivity: a brand new approach targeting cancer metabolism. Human Cell 36, 1441–1450 (2023). https://doi.org/10.1007/s13577-023-00896-5

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