Induction of ferroptosis by photodynamic therapy and enhancement of antitumor effect with ferroptosis inducers.
Ferroptosis
Lipid peroxidation
Photodynamic therapy
System xc−
Talaporfin sodium
Journal
Journal of gastroenterology
ISSN: 1435-5922
Titre abrégé: J Gastroenterol
Pays: Japan
ID NLM: 9430794
Informations de publication
Date de publication:
10 Nov 2023
10 Nov 2023
Historique:
received:
07
07
2023
accepted:
19
10
2023
medline:
10
11
2023
pubmed:
10
11
2023
entrez:
10
11
2023
Statut:
aheadofprint
Résumé
Photodynamic therapy (PDT) is an effective tumor treatment that involves the administration of a photosensitizer to generate cytotoxic Cell viability assay in TS-PDT-treated cells in combination with a ferroptosis inhibitor (ferrostatin-1: Fer-1) or ferroptosis inducers (imidazole ketone erastin: IKE, Ras-selective lethal 3: RSL3) was performed. Accumulation of lipid peroxidation, GPX4 antioxidant system and cystine/glutamate antiporter (system xc TS-PDT-induced cell death was partly suppressed by Fer-1 and accompanied by lipid peroxidation. TS-PDT combined with IKE or RSL3 enhanced the induction of cell death. TS-PDT inhibited cystine uptake activity via system xc This study found that the mechanism underlying TS-PDT-induced ferroptosis constitutes direct lipid peroxidation by the generated ROS, and the inhibition of system xc
Sections du résumé
BACKGROUND
BACKGROUND
Photodynamic therapy (PDT) is an effective tumor treatment that involves the administration of a photosensitizer to generate cytotoxic
METHODS
METHODS
Cell viability assay in TS-PDT-treated cells in combination with a ferroptosis inhibitor (ferrostatin-1: Fer-1) or ferroptosis inducers (imidazole ketone erastin: IKE, Ras-selective lethal 3: RSL3) was performed. Accumulation of lipid peroxidation, GPX4 antioxidant system and cystine/glutamate antiporter (system xc
RESULTS
RESULTS
TS-PDT-induced cell death was partly suppressed by Fer-1 and accompanied by lipid peroxidation. TS-PDT combined with IKE or RSL3 enhanced the induction of cell death. TS-PDT inhibited cystine uptake activity via system xc
CONCLUSION
CONCLUSIONS
This study found that the mechanism underlying TS-PDT-induced ferroptosis constitutes direct lipid peroxidation by the generated ROS, and the inhibition of system xc
Identifiants
pubmed: 37947872
doi: 10.1007/s00535-023-02054-y
pii: 10.1007/s00535-023-02054-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Society for the Promotion of Science London
ID : 20K08361
Organisme : Japan Society for the Promotion of Science London
ID : 23K07358
Organisme : Japan Society for the Promotion of Science London
ID : 22K20862
Organisme : Japan Society for the Promotion of Science London
ID : 23K15019
Organisme : Japan Society for the Promotion of Science London
ID : 23K07421
Organisme : Toyoaki Scholarship Foundation
ID : JOSE203179
Organisme : Iketani Science and Technology Foundation
ID : JOSE204007
Organisme : Bristol-Myers Squibb Foundation
ID : JOSE202103
Informations de copyright
© 2023. Japanese Society of Gastroenterology.
Références
Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer. 2003;3:380–7.
doi: 10.1038/nrc1071
pubmed: 12724736
Agostinis P, Berg K, Cengel KA, et al. Photodynamic therapy of cancer: an update. CA A Cancer J Clin. 2011. https://doi.org/10.3322/caac.20114 .
doi: 10.3322/caac.20114
Brown SB, Brown EA, Walker I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 2004;5:497–508.
doi: 10.1016/S1470-2045(04)01529-3
pubmed: 15288239
Yano T, Minamide T, Takashima K, et al. Clinical practice of photodynamic therapy using talaporfin sodium for esophageal cancer. J Clin Med. 2021. https://doi.org/10.3390/jcm10132785 .
doi: 10.3390/jcm10132785
pubmed: 35011798
pmcid: 8745312
Yano T, Kasai H, Horimatsu T, et al. A multicenter phase II study of salvage photodynamic therapy using talaporfin sodium (ME2906) and a diode laser (PNL6405EPG) for local failure after chemoradiotherapy or radiotherapy for esophageal cancer. Oncotarget. 2017;8:22135–44.
doi: 10.18632/oncotarget.14029
pubmed: 28212527
Dang J, He H, Chen D, et al. Manipulating tumor hypoxia toward enhanced photodynamic therapy (PDT). Biomater Sci. 2017;5:1500–11.
doi: 10.1039/C7BM00392G
pubmed: 28681887
Li RQ, Zhang C, Xie BR, et al. A two-photon excited O(2)-evolving nanocomposite for efficient photodynamic therapy against hypoxic tumor. Biomaterials. 2019;194:84–93.
doi: 10.1016/j.biomaterials.2018.12.017
pubmed: 30583151
Liu LH, Zhang YH, Qiu WX, et al. Dual-stage light amplified photodynamic therapy against hypoxic tumor based on an O(2) self-sufficient nanoplatform. Small. 2017. https://doi.org/10.1002/smll.201701621 .
doi: 10.1002/smll.201701621
pubmed: 29283218
pmcid: 5884067
Liu WL, Liu T, Zou MZ, et al. Aggressive man-made red blood cells for hypoxia-resistant photodynamic therapy. Adv Mater (Deerfield Beach, Fla). 2018;30:e1802006.
doi: 10.1002/adma.201802006
Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149:1060–72.
doi: 10.1016/j.cell.2012.03.042
pubmed: 22632970
pmcid: 3367386
Martin-Sanchez D, Ruiz-Andres O, Poveda J, et al. Ferroptosis, but not necroptosis, is important in nephrotoxic folic acid-induced AKI. J Am Soc Nephrol. 2017;28:218–29.
doi: 10.1681/ASN.2015121376
pubmed: 27352622
Carlson BA, Tobe R, Yefremova E, et al. Glutathione peroxidase 4 and vitamin E cooperatively prevent hepatocellular degeneration. Redox Biol. 2016;9:22–31.
doi: 10.1016/j.redox.2016.05.003
pubmed: 27262435
pmcid: 4900515
Guiney SJ, Adlard PA, Bush AI, et al. Ferroptosis and cell death mechanisms in Parkinson’s disease. Neurochem Int. 2017;104:34–48.
doi: 10.1016/j.neuint.2017.01.004
pubmed: 28082232
Wu X, Li Y, Zhang S, et al. Ferroptosis as a novel therapeutic target for cardiovascular disease. Theranostics. 2021;11:3052–9.
doi: 10.7150/thno.54113
pubmed: 33537073
pmcid: 7847684
Carneiro BA, El-Deiry WS. Targeting apoptosis in cancer therapy. Nat Rev Clin Oncol. 2020;17:395–417.
doi: 10.1038/s41571-020-0341-y
pubmed: 32203277
pmcid: 8211386
Viswanathan VS, Ryan MJ, Dhruv HD, et al. Dependency of a therapy-resistant state of cancer cells on a lipid peroxidase pathway. Nature. 2017;547:453–7.
doi: 10.1038/nature23007
pubmed: 28678785
pmcid: 5667900
Hangauer MJ, Viswanathan VS, Ryan MJ, et al. Drug-tolerant persister cancer cells are vulnerable to GPX4 inhibition. Nature. 2017;551:247–50.
doi: 10.1038/nature24297
pubmed: 29088702
pmcid: 5933935
Jiang X, Stockwell BR, Conrad M. Ferroptosis: mechanisms, biology and role in disease. Nat Rev Mol Cell Biol. 2021;22:266–82.
doi: 10.1038/s41580-020-00324-8
pubmed: 33495651
pmcid: 8142022
Yang WS, Stockwell BR. Ferroptosis: death by lipid peroxidation. Trends Cell Biol. 2016;26:165–76.
doi: 10.1016/j.tcb.2015.10.014
pubmed: 26653790
Zhu T, Shi L, Yu C, et al. Ferroptosis promotes photodynamic therapy: supramolecular photosensitizer-inducer nanodrug for enhanced cancer treatment. Theranostics. 2019;9:3293–307.
doi: 10.7150/thno.32867
pubmed: 31244955
pmcid: 6567978
Xu T, Ma Y, Yuan Q, et al. enhanced ferroptosis by oxygen-boosted phototherapy based on a 2-in-1 nanoplatform of ferrous hemoglobin for tumor synergistic therapy. ACS Nano. 2020;14:3414–25.
doi: 10.1021/acsnano.9b09426
pubmed: 32155051
Miotto G, Rossetto M, Di Paolo ML, et al. Insight into the mechanism of ferroptosis inhibition by ferrostatin-1. Redox Biol. 2020;28:101328.
doi: 10.1016/j.redox.2019.101328
pubmed: 31574461
Karuppagounder SS, Alin L, Chen Y, et al. N-acetylcysteine targets 5 lipoxygenase-derived, toxic lipids and can synergize with prostaglandin E(2) to inhibit ferroptosis and improve outcomes following hemorrhagic stroke in mice. Ann Neurol. 2018;84:854–72.
doi: 10.1002/ana.25356
pubmed: 30294906
pmcid: 6519209
Slee EA, Zhu H, Chow SC, et al. Benzyloxycarbonyl-Val-Ala-Asp (OMe) fluoromethylketone (Z-VAD.FMK) inhibits apoptosis by blocking the processing of CPP32. Biochem J. 1996. https://doi.org/10.1042/bj3150021 .
doi: 10.1042/bj3150021
pubmed: 8670109
pmcid: 1217173
Mikuš P, Pecher D, Rauová D, et al. Determination of novel highly effective necrostatin Nec-1s in rat plasma by high performance liquid chromatography hyphenated with quadrupole-time-of-flight mass spectrometry. Molecules (Basel, Switzerland). 2018. https://doi.org/10.3390/molecules23081946 .
doi: 10.3390/molecules23081946
pubmed: 30081531
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif). 2001;25:402–8.
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Dixon SJ, Patel DN, Welsch M, et al. Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. Elife. 2014. https://doi.org/10.7554/eLife.02523 .
doi: 10.7554/eLife.02523
pubmed: 24844246
pmcid: 4054777
Sengupta A, Lichti UF, Carlson BA, et al. Targeted disruption of glutathione peroxidase 4 in mouse skin epithelial cells impairs postnatal hair follicle morphogenesis that is partially rescued through inhibition of COX-2. J Invest Dermatol. 2013;133:1731–41.
doi: 10.1038/jid.2013.52
pubmed: 23364477
pmcid: 3652900
Shimomura T, Hirakawa N, Ohuchi Y, et al. Simple fluorescence assay for cystine uptake via the xCT in cells using selenocystine and a fluorescent probe. ACS Sensors. 2021;6:2125–8.
doi: 10.1021/acssensors.1c00496
pubmed: 34080411
Koppula P, Zhuang L, Gan B. Cystine transporter SLC7A11/xCT in cancer: ferroptosis, nutrient dependency, and cancer therapy. Protein Cell. 2021;12:599–620.
doi: 10.1007/s13238-020-00789-5
pubmed: 33000412
Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem Photobiol Sci Off J Eur Photochem Assoc Eur Soc Photobiol. 2002;1:1–21.
Aniogo EC, George BPA, Abrahamse H. Role of Bcl-2 family proteins in photodynamic therapy mediated cell survival and regulation. Molecules (Basel, Switzerland). 2020. https://doi.org/10.3390/molecules25225308 .
doi: 10.3390/molecules25225308
pubmed: 33203053
Miki Y, Akimoto J, Moritake K, et al. Photodynamic therapy using talaporfin sodium induces concentration-dependent programmed necroptosis in human glioblastoma T98G cells. Lasers Med Sci. 2015;30:1739–45.
doi: 10.1007/s10103-015-1783-9
pubmed: 26109138
Song R, Li T, Ye J, et al. Acidity-activatable dynamic nanoparticles boosting ferroptotic cell death for immunotherapy of cancer. Adv Mater (Deerfield Beach, Fla). 2021;33:e2101155.
doi: 10.1002/adma.202101155
Zhou Y, Chen K, Lin WK, et al. Photo-enhanced synergistic induction of ferroptosis for anti-cancer immunotherapy. Adv Healthc Mater. 2023. https://doi.org/10.1002/adhm.202300994 .
doi: 10.1002/adhm.202300994
pubmed: 37940192
Chen Q, Ma X, Xie L, et al. Iron-based nanoparticles for MR imaging-guided ferroptosis in combination with photodynamic therapy to enhance cancer treatment. Nanoscale. 2021;13:4855–70.
doi: 10.1039/D0NR08757B
pubmed: 33624647
Plaetzer K, Kiesslich T, Krammer B, et al. Characterization of the cell death modes and the associated changes in cellular energy supply in response to AlPcS4-PDT. Photochem Photobiol Sci Off J Eur Photochem Assoc Eur Soc Photobiol. 2002;1:172–7.
Hassannia B, Vandenabeele P, Vanden BT. Targeting ferroptosis to iron out cancer. Cancer Cell. 2019;35:830–49.
doi: 10.1016/j.ccell.2019.04.002
pubmed: 31105042
Ye LF, Chaudhary KR, Zandkarimi F, et al. Radiation-induced lipid peroxidation triggers ferroptosis and synergizes with ferroptosis inducers. ACS Chem Biol. 2020;15:469–84.
doi: 10.1021/acschembio.9b00939
pubmed: 31899616
pmcid: 7180072
Lei G, Zhang Y, Koppula P, et al. The role of ferroptosis in ionizing radiation-induced cell death and tumor suppression. Cell Res. 2020;30:146–62.
doi: 10.1038/s41422-019-0263-3
pubmed: 31949285
pmcid: 7015061
Shui S, Zhao Z, Wang H, et al. Non-enzymatic lipid peroxidation initiated by photodynamic therapy drives a distinct ferroptosis-like cell death pathway. Redox Biol. 2021;45:102056.
doi: 10.1016/j.redox.2021.102056
pubmed: 34229160
pmcid: 8264218
Turubanova VD, Balalaeva IV, Mishchenko TA, et al. Immunogenic cell death induced by a new photodynamic therapy based on photosens and photodithazine. J Immunother Cancer. 2019;7:350.
doi: 10.1186/s40425-019-0826-3
pubmed: 31842994
pmcid: 6916435
Lang X, Green MD, Wang W, et al. Radiotherapy and Immunotherapy promote tumoral lipid oxidation and ferroptosis via synergistic repression of SLC7A11. Cancer Discov. 2019;9:1673–85.
doi: 10.1158/2159-8290.CD-19-0338
pubmed: 31554642
pmcid: 6891128
Tanaka M, Sasaki M, Suzuki T, et al. Combination of talaporfin photodynamic therapy and Poly (ADP-Ribose) polymerase (PARP) inhibitor in gastric cancer. Biochem Biophys Res Commun. 2021;539:1–7.
doi: 10.1016/j.bbrc.2020.12.073
pubmed: 33388624
Seibt TM, Proneth B, Conrad M. Role of GPX4 in ferroptosis and its pharmacological implication. Free Radical Biol Med. 2019;133:144–52.
doi: 10.1016/j.freeradbiomed.2018.09.014
Stockwell BR, Jiang X. The chemistry and biology of ferroptosis. Cell Chem Biol. 2020;27:365–75.
doi: 10.1016/j.chembiol.2020.03.013
pubmed: 32294465
pmcid: 7204503
Sato H, Shiiya A, Kimata M, et al. Redox imbalance in cystine/glutamate transporter-deficient mice. J Biol Chem. 2005;280:37423–9.
doi: 10.1074/jbc.M506439200
pubmed: 16144837