Pro-survival and pro-growth effects of stress-induced nitric oxide in a prostate cancer photodynamic therapy model
Open accessAbstract
We discovered recently that human breast cancer cells subjected to photodynamic therapy (PDT)-like oxidative stress localized in mitochondria rapidly upregulated nitric oxide synthase-2 (NOS2) and nitric oxide (NO), which increased resistance to apoptotic photokilling. In this study, we asked whether human prostate cancer PC-3 cells would exploit NOS2/NO similarly and, if so, how proliferation of surviving cells might be affected. Irradiation of photosensitized PC-3 cells resulted in a rapid (<1 h), robust (~12-fold), and prolonged (∼20 h) post-irradiation upregulation of NOS2. Caspase-3/7 activation and apoptosis were stimulated by NOS2 inhibitors and a NO scavenger, implying that induced NO was acting cytoprotectively. Cyclic GMP involvement was ruled out, whereas suppression of pro-apoptotic JNK and p38 MAPK activation was clearly implicated. Cells surviving photostress grew back ~2-times faster than controls. NOS2 inhibition prevented this and the large increase in cell cycle S-phase occupancy observed after irradiation. Thus, photostress upregulation of NOS/NO elicited both a pro-survival and pro-growth response, both of which could compromise clinical PDT efficacy unless suppressed, e.g. by pharmacological intervention with a NOS2 inhibitor.
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Increased NO production after low doses of ALA-PDT with less than ~25% cell killing not only prevented tumor cell death but also made surviving tumor cells more proliferative and migratory.
“Such increased NO production, which occurred after low doses of ALA-PDT with less than ~25% cell killing, not only prevented tumor cell death but also made surviving tumor cells more proliferative and migratory [144,145,146].”
From 5-Aminolevulinic Acid as a Theranostic Agent for Tumor Fluorescence Imaging and Photodynamic Therapy (2023) · cites this paper as [144]
Results §3.3 reports that ALA/light-stressed PC-3 cells induced NOS2 and NO, which protected them against apoptotic death; Results §3.6 reports faster NO-dependent growth among surviving cells. The paper does not report increased migration or establish the claimed threshold of less than ~25% cell killing. Its ~25% figure in §3.6 describes growth in an inhibitor-treated group, not cell killing. (LLM, conf=0.87)
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Girotti, A. W., Bazak, J., & Korytowski, W. (2023) · Preprints.org · doi:10.20944/preprints202304.0819.v1 · Cited by 4 · see citing works
Self-citationKorbelik, M., Girotti, A. W., & Kessel, D. H. (2026) · Journal of Molecular Medicine · doi:10.1007/s00109-026-02651-3 · Cited by 3 · see citing works
Self-citationProduction and Role of Nitric Oxide in Endometrial Cancer
Yeo, S. G., Oh, Y. J., Lee, J. M., Yeo, J. H., Kim, S. S., & Park, D. C. (2025) · Antioxidants · doi:10.3390/antiox14030369 · Cited by 3 · see citing works
Girotti, A. W., & Korbelik, M. (2025) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-025-00817-5 · Cited by 2 · see citing works
Self-citationBazak, J., Korytowski, W., & Girotti, A. W. (2022) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2022040016 · Cited by 2 · see citing works
Self-citationFil, M., Lach, M., Bazak, J., Sarna, M., Girotti, A. W., & Korytowski, W. (2026) · Photochemical & Photobiological Sciences · doi:10.1007/s43630-026-00885-1 · Cited by 1 · see citing works
Self-citationPhotodynamic Therapy and Nitric Oxide
Pietra, E. D., & Rapozzi, V. (2015) · Springer eBooks · doi:10.1007/978-3-319-13611-0_14 · Cited by 1 · see citing works
Emerging Role of NO-Mediated Therapeutics
McCrudden, C. M., & McCarthy, H. O. (2015) · Springer eBooks · doi:10.1007/978-3-319-13611-0_13
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Self-citationPhotodynamic therapy of malignant brain gliomas
Розуменко, В. Д., Liubich, L. D., Петровна, С. Л., Михайловна, Е. Д., Малышева, Т. А., & Dashchakovskyi, A. V. (2022) · Ukrainian Neurosurgical Journal · doi:10.25305/unj.263389
Korytowski, W., Fil, M., Lach, M., Bazak, J., Sarna, M., & Girotti, A. W. (2025) · SSRN Electronic Journal · doi:10.2139/ssrn.5258505
Self-citation
- Authors
- Bhowmick, R., & Girotti, A. W.
- Affiliations
- Medical College of Wisconsin (US)
- Corresponding author
- Bhowmick, Reshma
- Girotti, Albert W.
- ORCID
- Girotti, Albert W.
- Venue
- Cancer Letters
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 343
- Issue
- 1
- Pages
- 115-122
- ISSN
- 0304-3835 (ISSN-L)
- PMC
- PMC3874260
- OpenAlex
- W2126780194
- Cited by
- 65
- References
- 48
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 8 · 2021: 3 · 2020: 6 · 2019: 7 · 2018: 3 · 2017: 5 · 2016: 8 · 2015: 8 · 2014: 5
- FWCI
- 5.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Letters (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (CA70823, R01CA070823)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- photodynamic therapy, nitric oxide, nitric oxide synthase 2, prostate cancer, PC-3 cells, oxidative stress, apoptosis resistance, cell survival, cell proliferation, JNK, p38 MAPK, S phase arrest, photosensitizers
- MeSH terms
- Cell Cycle, Cell Survival, Enzyme Activation, Free Radicals, Humans, Light, Male, Nitric Oxide, Photochemotherapy, Prostatic Neoplasms, Apoptosis, MAP Kinase Signaling System, Cell Line, Tumor, Cell Proliferation, Nitric Oxide Synthase Type II, Caspase 3, Caspase 7
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