Upstream signaling events leading to elevated production of pro-survival nitric oxide in photodynamically-challenged glioblastoma cells
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Nitric oxide (NO) generated endogenously by inducible nitric oxide synthase (iNOS) promotes growth and migration/invasion of glioblastoma cells and also fosters resistance to chemotherapy and ionizing radiotherapy. Our recent studies revealed that glioblastoma cell iNOS/NO also opposes the cytotoxic effects of non-ionizing photodynamic therapy (PDT), and moreover stimulates growth/migration aggressiveness of surviving cells. These negative responses, which depended on PI3K/Akt/NF-κB activation, were strongly suppressed by blocking iNOS transcription with JQ1, a BET bromodomain inhibitor. In the present study, we sought to identify additional molecular events that precede iNOS transcriptional upregulation. Akt activation, iNOS induction, and viability loss in PDT-challenged glioblastoma U87 cells were all strongly inhibited by added l-histidine, consistent with primary involvement of photogenerated singlet oxygen (1 O 2). Transacetylase p300 not only underwent greater Akt-dependent activation after PDT, but greater interaction with NF-κB subunit p65, which in turn exhibited greater K310 acetylation. In addition, PDT promoted intramolecular disulfide formation and inactivation of tumor suppressor PTEN, thereby favoring Akt and p300 activation leading to iNOS upregulation. Importantly, deacetylase Sirt1 was down-regulated by PDT stress, consistent with the observed increase in p65-acK310 level, which fostered iNOS transcription. This study provides new mechanistic insights into how glioblastoma tumors can exploit iNOS/NO to not only resist PDT, but to attain a more aggressive survival phenotype.
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The cause for this phenomenon was shown due to the activation of PI3K and NF-κB pathways, inhibition of which dampened the NO production and its negative biological consequences.
“Although how PDT-induced NO promotes tumor cell survival and invasiveness remains an open question, the cause for this phenomenon was shown due to the activation of PI3K and NF-κB pathways, inhibition of which dampened the NO production and its negative biological consequences [143,147,148].”
From 5-Aminolevulinic Acid as a Theranostic Agent for Tumor Fluorescence Imaging and Photodynamic Therapy (2023) · cites this paper as [148]
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Girotti, A. W., & Korytowski, W. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115697 · Cited by 12 · see citing works
Self-citationNitric oxide-elicited resistance to anti-glioblastoma photodynamic therapy
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Negative effects of tumor cell nitric oxide on anti-glioblastoma photodynamic therapy
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Pathak, A., Palasalava, S., Knott, M. V., Colon, B., Ciervo, E., Zhou, Y., Mitchell, J., Pumar, O. T., Wong, H. K. A., Zhang, L., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.18.603996 · Cited by 5 · see citing works
Pro-tumor Bystander Effects of Nitric Oxide in Anti-tumor Photodynamic TherapyPreprint
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Gayathri, S., Riyas, Z. M., & Christy, A. J. (2026) · Journal of the Indian Chemical Society · doi:10.1016/j.jics.2026.102532 · Cited by 1 · see citing works
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Photodynamic 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
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Self-citationShayan, S., Kuschman, H. P., Kevil, C. G., & Thomas, D. D. (2026) · Redox Biology · doi:10.1016/j.redox.2026.104344
- Authors
- Fahey, J. M., Korytowski, W., & Girotti, A. W.
- Affiliations
- Medical College of Wisconsin (US)
- Jagiellonian University (PL)
- Corresponding author
- Girotti, Albert W.
- Venue
- Free Radical Biology and Medicine
- Publisher
- Elsevier BV
- Published
- 2019-06
- Volume
- 137
- Pages
- 37-45
- ISSN
- 0891-5849 (ISSN-L)
- PMC
- PMC6526063
- OpenAlex
- W2937908663
- Cited by
- 38
- References
- 73
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 6 · 2023: 7 · 2022: 5 · 2021: 6 · 2020: 5 · 2019: 3
- FWCI
- 3.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Free Radical Biology and Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Homo Politicus (Academy of Humanities and Economics in Lodz) (submittedVersion, cc-by-nc-nd)
- Funders
- NIH (CA70823)
- NCI (5520347)
- BSC (3308239-FP12605)
- NCN (2017/27/B/NZ5/02620)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- glioblastoma, photodynamic therapy, nitric oxide, inducible nitric oxide synthase, singlet oxygen, PI3K/Akt signaling, NF-κB p65 acetylation, P300, PTEN inactivation, SIRT1, 5-aminolevulinic acid, JQ1, BET inhibitors, histidine, cell survival, drug resistance
- MeSH terms
- Cell Survival, Glioblastoma, Humans, Neoplasm Invasiveness, Nitric Oxide, Phosphorylation, Photochemotherapy, Signal Transduction, Transcriptional Activation, NF-kappa B, Cell Line, Tumor, Cell Proliferation, E1A-Associated p300 Protein, Nitric Oxide Synthase Type II
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