Hyperresistance to photosensitized lipid peroxidation and apoptotic killing in 5-aminolevulinate-treated tumor cells overexpressing mitochondrial GPX4
Abstract
Antitumor photodynamic therapy (PDT) with administered 5-aminolevulinic acid (ALA) is based on metabolism of ALA to protoporphyrin IX (PpIX), which acts as a sensitizer of photo-oxidative damage leading to apoptotic or necrotic cell death. An initial goal of this study was to ascertain how the PpIX-sensitized death mechanism for a breast tumor line (COH-BR1 cells) might be influenced by the conditions of ALA exposure in vitro. Two different treatment protocols were developed for addressing this question: (i) continuous incubation with 1 mM ALA for 90 min; and, (ii) discontinuous incubation, i.e., 15 min with 1 mM ALA followed by 225 min without it. Following exposure to 2 J/cm2 of visible light, cell viability, death mechanism, and lipid hydroperoxide (LOOH) level were evaluated for each protocol using thiazolyl blue, Hoechst staining, and HPLC with electrochemical detection assays, respectively. PpIX was found to sensitize apoptosis when it existed mainly in mitochondria (protocol-1), but necrosis when it diffused to other sites, including plasma membrane (protocol-2). Experiments with a transfectant clone, 7G4, exhibiting approximately 85 times greater activity of the LOOH-detoxifying selenoenzyme GPX4 than parental cells, provided additional information about death mechanism. Located predominantly in mitochondria of 7G4 cells, GPX4 strongly inhibited both LOOH accumulation and apoptosis under protocol-1 conditions, but had no significant effect under protocol-2 conditions. These findings support the hypothesis that LOOHs produced by attack of photogenerated singlet oxygen on mitochondrial membrane lipids play an important early role in the apoptotic death cascade.
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PDT when ALA-induced PpIX is localized in mitochondria or ER typically activates apoptotic pathways, whereas PDT when PpIX is in the plasma membrane often leads to necrosis.
“PDT at a time when ALA-induced PpIX is localized in mitochondria or ER typically activates apoptotic pathways, whereas PDT at a time when PpIX is in the plasma membrane often leads to necrosis [31].”
From 5-Aminolevulinic Acid as a Theranostic Agent for Tumor Fluorescence Imaging and Photodynamic Therapy (2023) · cites this paper as [31]
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Kriska, T., Levchenko, V., Chu, F., Esworthy, R. S., & Girotti, A. W. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.05.022 · Cited by 7 · see citing works
Self-citationOverchuk, M., Rickard, B. P., Tulino, J., Tan, X. M., Ligler, F. S., Huang, H., & Rizvi, I. (2024) · Photochemistry and Photobiology · doi:10.1111/php.13967 · Cited by 6 · see citing works
Apoptosis‐accommodating Effect of Nitric Oxide in Photodynamically Stressed Tumor Cells
Niziolek, M., Pilat, A. K., Korytowski, W., & Girotti, A. W. (2010) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2010.00712.x · Cited by 6 · see citing works
Self-citationKorytowski, W., Niziolek, M., & Girotti, A. W. (2005) · Analytical Biochemistry · doi:10.1016/j.ab.2005.04.005 · Cited by 6 · see citing works
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Self-citationAdigbli, D. K., Pye, H., Seebaluck, J., Loizidou, M., & MacRobert, A. J. (2019) · RSC Advances · doi:10.1039/c9ra04430b · Cited by 4 · see citing works
Enzymatic Oxidants, Antioxidants, and Inflammatory Bowel Disease
Esworthy, R. S. (2025) · Applied Biosciences · doi:10.3390/applbiosci4020019 · Cited by 5 · see citing works
Ran, Q., & Liang, H. (2011) · Humana Press eBooks · doi:10.1007/978-1-60761-956-7_12 · Cited by 2 · see citing works
A study of glutathione peroxidase 4 function in human intestinal epithelial cells
Ezea, P. C. (2013) · Cited by 1 · see citing works
Overchuk, M., Choi, A. M., Rickard, B. P., Schnoor, B., Ehrmann, B. M., Girotti, A. W., Huang, H., O’Connell, T. M., Gomez, S. M., & Rizvi, I. (2026) · Optical Biopsy: Toward Real-Time Spectroscopic Imaging and Diagnosis · doi:10.1117/12.3100970
Self-citation
- Authors
- Kriska, T., Korytowski, W., & Girotti, A. W.
- Affiliations
- Jagiellonian University (PL)
- Medical College of Wisconsin (US)
- Corresponding author
- Girotti, Albert W
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2002-11
- Volume
- 33
- Issue
- 10
- Pages
- 1389-1402
- ISSN
- 0891-5849 (ISSN-L)
- OpenAlex
- W2066747562
- Cited by
- 59
- References
- 59
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 1 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 1 · 2016: 3 · 2015: 2 · 2013: 5
- FWCI
- 3.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service
- National Cancer Institute (R01CA072630, CA 72630)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- photodynamic therapy, 5-aminolevulinic acid, protoporphyrin IX, GPX4, lipid peroxidation, lipid hydroperoxides, apoptosis, necrosis, mitochondrial membrane lipids, singlet oxygen, selenoenzymes
- MeSH terms
- Phospholipid Hydroperoxide Glutathione Peroxidase, Aminolevulinic Acid, Breast Neoplasms, Cell Survival, Flow Cytometry, Free Radicals, Glutathione Peroxidase, Humans, Lipid Peroxides, Microscopy, Fluorescence, Mitochondria, Phospholipids, Photochemotherapy, Porphyrins, Protoporphyrins, Subcellular Fractions, Time Factors, Transfection, Tumor Cells, Cultured, Lipid Peroxidation, Apoptosis, Photosensitizing Agents, Microscopy, Confocal, Rhodamine 123
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