Antagonistic Effects of Endogenous Nitric Oxide in a Glioblastoma Photodynamic Therapy Model
Open accessAbstract
Gliomas are aggressive brain tumors that are resistant to conventional chemotherapy and radiotherapy. Much of this resistance is attributed to endogenous nitric oxide (NO). Recent studies revealed that 5‐aminolevulinic acid (ALA)‐based photodynamic therapy (PDT) has advantages over conventional treatments for glioblastoma. In this study, we used an in vitro model to assess whether NO from glioblastoma cells can interfere with ALA‐PDT. Human U87 and U251 cells expressed significant basal levels of neuronal NO synthase (nNOS) and its inducible counterpart (iNOS). After an ALA/light challenge, iNOS level increased three‐ to fourfold over 24 h, whereas nNOS remained unchanged. Elevated iNOS resulted in a large increase in intracellular NO. Extent of ALA/light‐induced apoptosis increased substantially when an iNOS inhibitor or NO scavenger was present, implying that iNOS/NO was acting cytoprotectively. Moreover, cells surviving a photochallenge exhibited a striking increase in proliferation, migration and invasion rates, iNOS/NO again playing a dominant role. Also observed was a large iNOS/NO‐dependent increase in matrix metalloproteinase‐9 activity, decrease in tissue inhibitor of metalloproteinase‐1 expression and increase in survivin and S100A4 expression, each effect being consistent with accelerated migration/invasion as a prelude to metastasis. Our findings suggest introduction of iNOS inhibitors as pharmacologic adjuvants for glioblastoma PDT.
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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 [145]
The Results report that iNOS/NO protected U87 and U251 glioblastoma cells against ALA/light-induced killing, and that surviving U87 cells showed NO-dependent increases in proliferation and migration. The experiments used a low light fluence of 1 J/cm², but the passages in our copy do not establish the claim’s specific threshold of less than ~25% cell killing. (LLM, conf=0.84)
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Cites
Mosmann, T. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90303-4 · Cited by 56,104 · see citing works
Vermes, I., Haanen, C., Steffens-Nakken, H. M., & Reutellingsperger, C. (1995) · Journal of Immunological Methods · doi:10.1016/0022-1759(95)00072-i · Cited by 5,437 · see citing works
Cillà, S. D., Farruggio, S., Vujosevic, S., Raina, G., Filippini, D. A., Gatti, V., Clemente, N., Mary, D., Vezzola, D., Casini, G., et al. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479441 · Cited by 5,154 · see citing works
Photodynamic therapy of cancer: An update
Agostinis, P., Berg, K., Cengel, K. A., Foster, T. H., Girotti, A. W., Gollnick, S. O., Hahn, S. M., Hamblin, M. R., Juzeniene, A., Kessel, D., et al. (2011) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.20114 · Cited by 5,145 · see citing works
Self-citationDougherty, T. J., Gomer, C. J., Henderson, B. W., Jori, G., Kessel, D., Korbelik, M., Moan, J., & Peng, Q. (1998) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/90.12.889 · Cited by 4,716 · see citing works
Wen, P. Y., & Kesari, S. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708126 · Cited by 4,200 · see citing works
Gomer, C. J. (1988) · Cited by 4,169 · see citing works
Nitric oxide synthases: structure, function and inhibition
ALDERTON, W. K., Cooper, C. E., & Knowles, R. G. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3570593 · Cited by 4,106 · see citing works
Bevacizumab Alone and in Combination With Irinotecan in Recurrent Glioblastoma
Friedman, H. S., Prados, M. D., Wen, P. Y., Mikkelsen, T., Schiff, D., Abrey, L. E., Yung, W. K. A., Paleologos, N. A., Nicholas, M. K., Jensen, R. L., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.19.8721 · Cited by 2,463 · see citing works
HOW DOES PHOTODYNAMIC THERAPY WORK?
Henderson, B. W., & Dougherty, T. J. (1992) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1992.tb04222.x · Cited by 2,376 · see citing works
Malignant astrocytic glioma: genetics, biology, and paths to treatment
Furnari, F. B., Fenton, T., Bachoo, R. M., Mukasa, A., Stommel, J. M., Stegh, A., Hahn, W. C., Ligon, K. L., Louis, D. N., Brennan, C., et al. (2007) · Genes & Development · doi:10.1101/gad.1596707 · Cited by 2,316 · see citing works
Primary brain tumours in adults
Ricard, D., Idbaïh, A., Ducray, F., Lahutte, M., Hoang‐Xuan, K., & Delattre, J. (2012) · The Lancet · doi:10.1016/s0140-6736(11)61346-9 · Cited by 1,200 · see citing works
In vitro cell migration and invasion assays
Kramer, N., Walzl, A., Unger, C., Rosner, M., Krupitza, G., Hengstschläger, M., & Dolznig, H. (2013) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2012.08.001 · Cited by 1,170 · see citing works
Survivin, cancer networks and pathway-directed drug discovery
Altieri, D. C. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2293 · Cited by 998 · see citing works
Wardman, P. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.06.026 · Cited by 863 · see citing works
Matrix metalloproteinases in tumor invasion and metastasis
Stamenkovic, I. (2000) · Seminars in Cancer Biology · doi:10.1006/scbi.2000.0379 · Cited by 809 · see citing works
Roles of nitric oxide in tumor growth.
Jenkins, D. C., Charles, I. G., Thomsen, L. L., Moss, D. W., Holmes, L., Baylis, S. A., Rhodes, P., Westmore, K., Emson, P. C., & Moncada, S. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.10.4392 · Cited by 781 · see citing works
Primary brain tumours in adults
Béhin, A., Hoang‐Xuan, K., Carpentier, A. F., & Delattre, J. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12328-8 · Cited by 756 · see citing works
Gelatinase-mediated migration and invasion of cancer cells
Björklund, M., & Koivunen, E. (2005) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2005.03.001 · Cited by 663 · see citing works
5-Aminolevulinic Acid-Based Photodynamic Therapy: Principles and Experimental Research
Peng, Q., Berg, K., Moan, J., Kongshaug, M., & Nesland, J. M. (1997) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1997.tb08549.x · Cited by 615 · see citing works
Radiotherapy for newly diagnosed malignant glioma in adults: a systematic review
Laperrière, N., Zuraw, L., & Cairncross, G. J. (2002) · Radiotherapy and Oncology · doi:10.1016/s0167-8140(02)00078-6 · Cited by 424 · see citing works
Boye, K., & Mælandsmo, G. M. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090526 · Cited by 413 · see citing works
Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin
Lechner, M., Lirk, P., & Rieder, J. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.04.004 · Cited by 410 · see citing works
The yin and yang of nitric oxide in cancer progression
Burke, A. J., Sullivan, F. J., Giles, F. J., & Glynn, S. A. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt034 · Cited by 372 · see citing works
S100A4, a Mediator of Metastasis
Garrett-Thomson, S. C., Varney, K. M., Weber, D. J., & Bresnick, A. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.r500017200 · Cited by 352 · see citing works
Zymography methods for visualizing hydrolytic enzymes
Vandooren, J., Geurts, N., Martens, E., den Steen, P. E. V., & Opdenakker, G. (2013) · Nature Methods · doi:10.1038/nmeth.2371 · Cited by 322 · see citing works
Glioma Stem Cell Proliferation and Tumor Growth Are Promoted by Nitric Oxide Synthase-2
Eyler, C. E., Wu, Q., Yan, K. K.-L., MacSwords, J., Chandler-Militello, D., Misuraca, K. L., Lathia, J. D., Forrester, M. T., Lee, J., Stamler, J. S., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.006 · Cited by 309 · see citing works
Olson, M. W., Gervasi, D. C., Mobashery, S., & Fridman, R. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.47.29975 · Cited by 288 · see citing works
Targeting survivin in cancer therapy: fulfilled promises and open questions
Pennati, M., Folini, M., & Zaffaroni, N. (2007) · Carcinogenesis · doi:10.1093/carcin/bgm047 · Cited by 230 · see citing works
Photodynamic therapy of high grade glioma – long term survival
Stylli, S. S., Kaye, A. H., MacGregor, L., Howes, M., & Rajendra, P. (2005) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2005.01.006 · Cited by 214 · see citing works
Photodynamic therapy (PDT) for malignant brain tumors – Where do we stand?
Quirk, B. J., Brandal, G., Donlon, S., Vera, J. C., Mang, T. S., Foy, A. B., Lew, S. M., Girotti, A. W., Jogal, S., LaViolette, P. S., et al. (2015) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2015.04.009 · Cited by 208 · see citing works
Self-citationHansel, T. T., Kharitonov, S. A., Donnelly, L. E., Erin, E. M., Currie, M. G., Moore, W. M., Manning, P. T., Recker, D. P., & Barnes, P. J. (2003) · The FASEB Journal · doi:10.1096/fj.02-0633fje · Cited by 208 · see citing works
Brain Tumor Stem Cells: Bringing Order to the Chaos of Brain Cancer
Dirks, P. B. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.17.6792 · Cited by 168 · see citing works
Yang, X., Palasuberniam, P., Kraus, D., & Chen, B. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161025865 · Cited by 158 · see citing works
Kiziltepe, T., Hideshima, T., Ishitsuka, K., Ocio, E. M., Raje, N. S., Catley, L. P., Li, C., Trudel, L. J., Yasui, H., Vallet, S., et al. (2007) · Blood · doi:10.1182/blood-2006-10-052845 · Cited by 146 · see citing works
Selective Inducible Nitric Oxide Synthase Inhibition has no Effect on Allergen Challenge in Asthma
Singh, D., Richards, D. B., Knowles, R. G., Schwartz, S., Woodcock, A. A., Langley, S., & O'Connor, B. J. (2007) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200704-588oc · Cited by 144 · see citing works
Bioimaging Probes for Reactive Oxygen Species and Reactive Nitrogen Species
Nagano, T. (2009) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.r09-66 · Cited by 143 · see citing works
Switzer, C. H., Glynn, S. A., Cheng, R. Y.-S., Ridnour, L. A., Green, J. E., Ambs, S., & Wink, D. A. (2012) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-12-0124 · Cited by 141 · see citing works
Expression of matrix metalloproteinases and their inhibitors in human brain tumors
Kachra, Z., Beaulieu, É., Delbecchi, L., Mousseau, N., Berthelet, F., Moumdjian, R. A., Maestro, R. F. D., & Béliveau, R. (1999) · Clinical & Experimental Metastasis · doi:10.1023/a:1006760632766 · Cited by 141 · see citing works
Photodynamic therapy of malignant brain tumours: A complementary approach to conventional therapies
Béchet, D., Mordon, S. R., Guillemin, F. H., & Barberi‐Heyob, M. (2012) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2012.07.004 · Cited by 137 · see citing works
Nitric oxide production by tumour tissue: impact on the response to photodynamic therapy
Korbelik, M., Parkins, C. S., Shibuya, H., Cecić, I., Stratford, M. R. L., & Chaplin, D. J. (2000) · British Journal of Cancer · doi:10.1054/bjoc.2000.1157 · Cited by 116 · see citing works
Ferrario, A., Rucker, N., Wong, S. S., Luna, M. C., & Gomer, C. J. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4785 · Cited by 116 · see citing works
Nitric oxide-matrix metaloproteinase-9 interactions: Biological and pharmacological significance
O’Sullivan, S., Medina, C., Ledwidge, M. T., Radomski, M. W., & Gilmer, J. F. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.12.006 · Cited by 112 · see citing works
The role of tumour-derived iNOS in tumour progression and angiogenesis
Kostourou, V., Cartwright, J. E., Johnstone, A. P., Boult, J. K. R., Cullis, E. R., Whitley, G. S. J., & Robinson, S. P. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6606034 · Cited by 99 · see citing works
Photoirradiation therapy of experimental malignant glioma with 5-aminolevulinic acid
Olzowy, B., Hundt, C., Stocker, S., Bise, K., Reulen, H. J., & Stummer, W. (2002) · Journal of neurosurgery · doi:10.3171/jns.2002.97.4.0970 · Cited by 92 · see citing works
Rapozzi, V., Pietra, E. D., & Bonavida, B. (2015) · Redox Biology · doi:10.1016/j.redox.2015.07.015 · Cited by 88 · see citing works
Disruption of the blood–brain barrier following ALA‐mediated photodynamic therapy
Hirschberg, H., Uzal, F. A., Chighvinadze, D., Zhang, M. J., Peng, Q., & Madsen, S. J. (2008) · Lasers in Surgery and Medicine · doi:10.1002/lsm.20670 · Cited by 86 · see citing works
Nitric oxide-mediated activity in anti-cancer photodynamic therapy
Rapozzi, V., Pietra, E. D., Zorzet, S., Zacchigna, M., Bonavida, B., & Xodo, L. E. (2013) · Nitric Oxide · doi:10.1016/j.niox.2013.01.002 · Cited by 84 · see citing works
Henderson, B. W., Sitnik, T. M., & Vaughan, L. A. (1999) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1999.tb01950.x · Cited by 79 · see citing works
Fahey, J. M., & Girotti, A. W. (2015) · Nitric Oxide · doi:10.1016/j.niox.2015.05.006 · Cited by 77 · see citing works
Self-citationInducible NO synthase confers chemoresistance in head and neck cancer by modulating survivin
Fetz, V., Bier, C., Habtemichael, N., Schuon, R., Schweitzer, A., Kunkel, M., Engels, K., Kovács, A. F., Schneider, S. S., Mann, W. J., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.24182 · Cited by 70 · see citing works
Hurst, R., Korytowski, W., Kriska, T., Esworthy, R. S., Chu, F., & Girotti, A. W. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00685-2 · Cited by 69 · see citing works
Self-citationBhowmick, R., & Girotti, A. W. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.12.005 · Cited by 67 · see citing works
Self-citationBhowmick, R., & Girotti, A. W. (2014) · Cancer Letters · doi:10.1016/j.canlet.2013.09.025 · Cited by 65 · see citing works
Self-citationiNOS: A Potential Therapeutic Target for Malignant Glioma
Jahani‐Asl, A., & Bonni, A. (2013) · Current Molecular Medicine · doi:10.2174/1566524011313080002 · Cited by 59 · see citing works
Kriska, T., Korytowski, W., & Girotti, A. W. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)01078-x · Cited by 59 · see citing works
Self-citationNOS‐2 signaling and cancer therapy
Bian, K., Ghassemi, F., Sotolongo, A., Siu, A., Shauger, L., Kots, A. Y., & Murad, F. (2012) · IUBMB Life · doi:10.1002/iub.1057 · Cited by 57 · see citing works
Heinrich, T. A., Tedesco, A. C., Fukuto, J. M., & da Silva, R. S. (2013) · Dalton Transactions · doi:10.1039/c3dt52217b · Cited by 53 · see citing works
Fractionated radiation‐induced nitric oxide promotes expansion of glioma stem‐like cells
Kim, R., Suh, Y., Cui, Y., Hwang, E., Lim, E., Yoo, K.-C., Lee, G., Yi, J., Kang, S., & Lee, S. (2013) · Cancer Science · doi:10.1111/cas.12207 · Cited by 49 · see citing works
Endogenously produced nitric oxide mitigates sensitivity of melanoma cells to cisplatin
Godoy, L. C., Anderson, C. C. T., Chowdhury, R., Trudel, L. J., & Wogan, G. N. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218938109 · Cited by 49 · see citing works
Etminan, N., Peters, C., Ficnar, J., Anlasik, S., Bünemann, E., Slotty, P. J., Hänggi, D., Steiger, H., Sorg, R. V., & Stummer, W. (2011) · Journal of neurosurgery · doi:10.3171/2011.3.jns10434 · Cited by 49 · see citing works
MMP-9 and uPAR regulated glioma cell migration
Veeravalli, K. K., & Rao, J. S. (2012) · Cell Adhesion & Migration · doi:10.4161/cam.21673 · Cited by 45 · see citing works
Applications for nitric oxide in halting proliferation of tumor cells
Reynolds, M. M., Witzeling, S. D., Damodaran, V. B., Medeiros, T. N., Knodle, R. D., Edwards, M. A., Lookian, P. P., & Brown, M. A. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.01.041 · Cited by 42 · see citing works
Bhowmick, R., & Girotti, A. W. (2010) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2010.00877.x · Cited by 40 · see citing works
Self-citationMalignant glioma progression and nitric oxide
Lam-Himlin, D. M., Espey, M. G., Perry, G. L., Smith, M. A., & Castellani, R. J. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2006.07.001 · Cited by 38 · see citing works
Bhowmick, R., & Girotti, A. W. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.06.009 · Cited by 36 · see citing works
Self-citationZhang, X., Jiang, F., Zhang, Z. G., Kalkanis, S. N., Hong, X., deCarvalho, A. C., Chen, J., Yang, H., Robin, A. M., & Chopp, M. (2005) · Lasers in Medical Science · doi:10.1007/s10103-005-0348-8 · Cited by 30 · see citing works
Clinical Studies with Targeted Toxins in Malignant Glioma
Rainov, N. G., & Söling, A. (2006) · Reviews on Recent Clinical Trials · doi:10.2174/157488706776876454 · Cited by 29 · see citing works
Bonavida, B., Baritaki, S., Huerta‐Yépez, S., Vega, M. I., Jazirehi, A. R., & Berenson, J. R. (2010) · Springer eBooks · doi:10.1007/978-1-4419-1432-3_24 · Cited by 22 · see citing works
High-Grade Glioma/Glioblastoma Multiforme: Is There a Role for Photodynamic Therapy?
Whelan, H. T. (2012) · Journal of the National Comprehensive Cancer Network · doi:10.6004/jnccn.2012.0171 · Cited by 16 · see citing works
Lancaster, J. R. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.06.015 · Cited by 13 · see citing works
Jin, T., Zhang, Z., Yang, X., & Luo, J.-S. (2015) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2015.16.7.2883 · Cited by 10 · see citing works
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- Authors
- Fahey, J. M., Emmer, J. V., Korytowski, W., Hogg, N., & Girotti, A. W.
- Affiliations
- Medical College of Wisconsin (US)
- Jagiellonian University (PL)
- Corresponding author
- Girotti, Albert W.
- Venue
- Photochemistry and Photobiology
- Publisher
- Wiley
- Published
- 2016-10-17
- Volume
- 92
- Issue
- 6
- Pages
- 842-853
- ISSN
- 0031-8655 (ISSN-L)
- 1751-1097
- PMC
- PMC5161550
- OpenAlex
- W2510529496
- Cited by
- 49
- References
- 72
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 5 · 2023: 8 · 2022: 3 · 2021: 5 · 2020: 5 · 2019: 6 · 2018: 5 · 2017: 1 · 2016: 3
- FWCI
- 4.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Photochemistry and Photobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Jagiellonian University Repository (Jagiellonian University) (submittedVersion, cc-by-nc-nd)
- Funders
- U.S. Public Health Service (CA70823)
- National Cancer Institute
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Photodynamic Therapy Research Studies
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Keywords
- glioblastoma, photodynamic therapy, 5-aminolevulinic acid, nitric oxide, inducible nitric oxide synthase, neuronal nitric oxide synthase, apoptosis, cell migration and invasion, MMP-9, TIMP-1, survivin, S100A4, iNOS inhibitors, NO scavenger, metastasis
- MeSH terms
- Adjuvants, Pharmaceutic, Aminolevulinic Acid, Animals, Cell Survival, Glioblastoma, Humans, Nitric Oxide, Photochemotherapy, Apoptosis, Cell Line, Tumor, Nitric Oxide Synthase Type II
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