Abstract
Bladder cancer (BC) is the most common cancer of the urinary tract and despite all innovations, remains a major challenge due to high morbidity and mortality. Genomic and epigenetic analyses allowed the discovery of new genes and pathways involved in the pathogenesis and regulation of BC. However, the effect on mortality has been modest and the development of new targets for BC treatment are needed. Recent evidence suggests that cancer cells are under increased stress associated with oncogenic transformation, with changes in metabolic activity and increased generation of reactive oxygen species (ROS). The increased amounts of ROS in cancer cells are associated with stimulation of cellular proliferation, promotion of mutations and genetic instability, as well as alterations in cellular sensitivity to anticancer agents. Since these mechanisms occur in cancer cells, there is a close link between oxidative stress (OS) and BC with implications in prevention, carcinogenesis, prognosis, and treatment. We address the role of OS as an enemy towards BC development, as well as an ally to fight against BC. This review promises to expand our treatment options for BC with OS-based therapies and launches this approach as an opportunity to improve our ability to select patients most likely to respond to personalized therapy.
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References
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492
Wong MCS, Fung FDH, Leung C, Cheung WWL, Goggins WB, Ng CF (2018) The global epidemiology of bladder cancer: a joinpoint regression analysis of its incidence and mortality trends and projection. Sci Rep 8:1129. https://doi.org/10.1038/s41598-018-19199-z
Saginala K, Barsouk A, Aluru JS, Rawla P, Padala SA, Barsouk A (2020) Epidemiology of bladder cancer. Med Sci 8:15. https://doi.org/10.3390/medsci8010015
Al-Zalabani AH, Stewart KFJ, Wesselius A, Schols AMWJ, Zeegers MP (2016) Modifiable risk factors for the prevention of bladder cancer: a systematic review of meta-analyses. Eur J Epidemiol 31:811–851. https://doi.org/10.1007/s10654-016-0138-6
Richters A, Aben KKH, Kiemeney LALM (2020) The global burden of urinary bladder cancer: an update. World J Urol 38:1895–1904. https://doi.org/10.1007/s00345-019-02984-4
Shin JH, Lim JS, Jeon BH (2018) Pathophysiology of bladder cancer. In Bladder Cancer. Elsevier, Amsterdam, pp 33–41 ISBN 9780128099407
Cheng L, Zhang S, MacLennan GT, Williamson SR, Lopez-Beltran A, Montironi R (2011) Bladder cancer: translating molecular genetic insights into clinical practice. Hum Pathol 42:455–481. https://doi.org/10.1016/j.humpath.2010.07.007
Naito S, Algaba F, Babjuk M, Bryan RT, Sun Y-H, Valiquette L, de la Rosette J (2016) The Clinical Research Office of the Endourological Society (CROES) multicentre randomised trial of narrow band imaging-assisted transurethral resection of bladder tumour (TURBT) versus conventional white light imaging-assisted TURBT in primary non–muscle-. Eur Urol 70:506–515. https://doi.org/10.1016/j.eururo.2016.03.053
Burger M, Catto JWF, Dalbagni G, Grossman HB, Herr H, Karakiewicz P, Kassouf W, Kiemeney LA, La Vecchia C, Shariat S et al (2013) Epidemiology and risk factors of urothelial bladder cancer. Eur Urol 63:234–241. https://doi.org/10.1016/j.eururo.2012.07.033
Babjuk M, Böhle A, Burger M, Capoun O, Cohen D, Compérat EM, Hernández V, Kaasinen E, Palou J, Rouprêt M et al (2017) EAU guidelines on non–muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol 71:447–461. https://doi.org/10.1016/j.eururo.2016.05.041
Bruce Bracken R, Swanson DA, Johnson DE, De Furia D, Von Eschenbach AC, Crooke S (1980) Role of intravesical mitomycin c in management of superficial bladder tumors. Urology 16:11–15. https://doi.org/10.1016/0090-4295(80)90322-2
Morales A, Eidinger D, Bruce AW (1976) Intracavitary bacillus calmette-guerin in the treatment of superficial bladder tumors. J Urol 116:180–182. https://doi.org/10.1016/S0022-5347(17)58737-6
Fradet Y, Bellmunt J, Vaughn DJ, Lee JL, Fong L, Vogelzang NJ, Climent MA, Petrylak DP, Choueiri TK, Necchi A et al (2019) Randomized phase III KEYNOTE-045 trial of pembrolizumab versus paclitaxel, docetaxel, or vinflunine in recurrent advanced urothelial cancer: results of >2 years of follow-up. Ann Oncol 30:970–976. https://doi.org/10.1093/annonc/mdz127
Powles T, Durán I, van der Heijden MS, Loriot Y, Vogelzang NJ, De Giorgi U, Oudard S, Retz MM, Castellano D, Bamias A et al (2018) Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. Lancet 391:748–757. https://doi.org/10.1016/S0140-6736(17)33297-X
Sharma P, Retz M, Siefker-Radtke A, Baron A, Necchi A, Bedke J, Plimack ER, Vaena D, Grimm M-O, Bracarda S et al (2017) Nivolumab in metastatic urothelial carcinoma after platinum therapy (CheckMate 275): a multicentre, single-arm, phase 2 trial. Lancet Oncol 18:312–322. https://doi.org/10.1016/S1470-2045(17)30065-7
von der Maase H, Sengelov L, Roberts JT, Ricci S, Dogliotti L, Oliver T, Moore MJ, Zimmermann A, Arning M (2005) Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J Clin Oncol 23:4602–4608. https://doi.org/10.1200/JCO.2005.07.757
Liu D, Qiu X, Xiong X, Chen X, Pan F (2020) Current updates on the role of reactive oxygen species in bladder cancer pathogenesis and therapeutics. Clin Transl Oncol 22:1687–1697. https://doi.org/10.1007/s12094-020-02330-w
Badjatia N, Satyam A, Singh P, Seth A, Sharma A (2010) Altered antioxidant status and lipid peroxidation in Indian patients with urothelial bladder carcinoma. Urol Oncol Semin Orig Investig 28:360–367. https://doi.org/10.1016/j.urolonc.2008.12.010
Sawicka E, Kratz EM, Szymańska B, Guzik A, Wesołowski A, Kowal P, Pawlik-Sobecka L, Piwowar A (2020) Preliminary study on selected markers of oxidative stress, inflammation and angiogenesis in patients with bladder cancer. Pathol Oncol Res 26:821–831. https://doi.org/10.1007/s12253-019-00620-5
Gecit İ, Eryılmaz R, Kavak S, Meral İ, Demir H, Pirinççi N, Güneş M, Taken K (2017) The prolidase activity, oxidative stress, and nitric oxide levels of bladder tissues with or without tumor in patients with bladder cancer. J Membr Biol 250:455–459. https://doi.org/10.1007/s00232-017-9971-0
Sosa V, Moliné T, Somoza R, Paciucci R, Kondoh H, Lleonart ME (2013) Oxidative stress and cancer: an overview. Ageing Res Rev 12:376–390. https://doi.org/10.1016/j.arr.2012.10.004
Liu Y, Li Q, Zhou L, Xie N, Nice EC, Zhang H, Huang C, Lei Y (2016) Cancer drug resistance: redox resetting renders a way. Oncotarget 7:42740–42761. https://doi.org/10.18632/oncotarget.8600
Ivanova D, Zhelev Z, Aoki I, Bakalova R, Higashi T (2016) Overproduction of reactive oxygen species—obligatory or not for induction of apoptosis by anticancer drugs. Chin J Cancer Res 28:383–396. https://doi.org/10.21147/j.issn.1000-9604.2016.04.01
Di Meo S, Reed TT, Venditti P, Victor VM (2016) Role of ROS and RNS sources in physiological and pathological conditions. Oxid Med Cell Longev 2016:1–44. https://doi.org/10.1155/2016/1245049
Tharmalingam S, Alhasawi A, Appanna VP, Lemire J, Appanna VD (2017) Reactive nitrogen species (RNS)-resistant microbes: adaptation and medical implications. Biol Chem 398:1193–1208. https://doi.org/10.1515/hsz-2017-0152
Grimm EA, Sikora AG, Ekmekcioglu S (2013) Molecular pathways: inflammation-associated nitric-oxide production as a cancer-supporting redox mechanism and a potential therapeutic target. Clin Cancer Res 19:5557–5563. https://doi.org/10.1158/1078-0432.CCR-12-1554
Lau N, Pluth MD (2019) Reactive sulfur species (RSS): persulfides, polysulfides, potential, and problems. Curr Opin Chem Biol 49:1–8. https://doi.org/10.1016/j.cbpa.2018.08.012
Gruhlke MCH, Slusarenko AJ (2012) The biology of reactive sulfur species (RSS). Plant Physiol Biochem 59:98–107. https://doi.org/10.1016/j.plaphy.2012.03.016
Olson KR, Gao Y, Arif F, Arora K, Patel S, DeLeon ER, Sutton TR, Feelisch M, Cortese-Krott MM, Straub KD (2018) Metabolism of hydrogen sulfide (H2S) and production of reactive sulfur species (RSS) by superoxide dismutase. Redox Biol 15:74–85. https://doi.org/10.1016/j.redox.2017.11.009
Cortese-Krott MM, Koning A, Kuhnle GGC, Nagy P, Bianco CL, Pasch A, Wink DA, Fukuto JM, Jackson AA, van Goor H et al (2017) The reactive species interactome: evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine. Antioxid Redox Signal 27:684–712. https://doi.org/10.1089/ars.2017.7083
Marengo B, Nitti M, Furfaro AL, Colla R, de Ciucis C, Marinari UM, Pronzato MA, Traverso N, Domenicotti C (2016) Redox homeostasis and cellular antioxidant systems: crucial players in cancer growth and therapy. Oxid Med Cell Longev 2016:1–16. https://doi.org/10.1155/2016/6235641
Mao S, Huang S (2013) Zinc and copper levels in bladder cancer: a systematic review and meta-analysis. Biol Trace Elem Res 153:5–10. https://doi.org/10.1007/s12011-013-9682-z
Whongsiri P, Pimratana C, Wijitsettakul U, Sanpavat A, Jindatip D, Hoffmann MJ, Goering W, Schulz WA, Boonla C (2019) Oxidative stress and LINE-1 reactivation in bladder cancer are epigenetically linked through active chromatin formation. Free Radic Biol Med 134:419–428. https://doi.org/10.1016/j.freeradbiomed.2019.01.031
Günes M, Eryilmaz R, Aslan R, Taken K, Demir H, Demir C (2020) Oxidant-antioxidant levels in patients with bladder tumours. Aging Male. https://doi.org/10.1080/13685538.2020.1718636
Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40. https://doi.org/10.1016/j.cbi.2005.12.009
Islam MO, Bacchetti T, Ferretti G (2019) Alterations of antioxidant enzymes and biomarkers of nitro-oxidative stress in tissues of bladder cancer. Oxid Med Cell Longev 2019:1–10. https://doi.org/10.1155/2019/2730896
Utangac MM, Yeni E, Savas M, Altunkol A, Ciftci H, Gumus K, Demir M (2017) Paraoxonase and arylesterase activity in bladder cancer. Türk Üroloji Dergisi/Turk J Urol 43:147–151. https://doi.org/10.5152/tud.2017.89411
Gecit I, Aslan M, Gunes M, Pirincci N, Esen R, Demir H, Ceylan K (2012) Serum prolidase activity, oxidative stress, and nitric oxide levels in patients with bladder cancer. J Cancer Res Clin Oncol 138:739–743. https://doi.org/10.1007/s00432-011-1136-4
Wongpaiboonwattana W, Tosukhowong P, Dissayabutra T, Mutirangura A, Boonla C (2013) Oxidative stress induces hypomethylation of LINE-1 and hypermethylation of the RUNX3 promoter in a bladder cancer cell line. Asian Pac J Cancer Prev 14:3773–3778. https://doi.org/10.7314/APJCP.2013.14.6.3773
Patchsung M, Boonla C, Amnattrakul P, Dissayabutra T, Mutirangura A, Tosukhowong P (2012) Long interspersed nuclear element-1 hypomethylation and oxidative stress: correlation and bladder cancer diagnostic potential. PLoS ONE 7:e37009. https://doi.org/10.1371/journal.pone.0037009
Whongsiri P, Pimratana C, Wijitsettakul U, Jindatip D, Sanpavat A, Schulz WA, Hoffmann MLJ, Goering W, Boonla C (2018) LINE-1 ORF1 protein is up-regulated by reactive oxygen species and associated with bladder urothelial carcinoma progression. Cancer Genomics Proteomics 15:143–151. https://doi.org/10.21873/cgp.20072
Kavitha S (2015) Cancer biology. In Viva voce in biochemistry, vol 168. Jaypee Brothers Medical Publishers (P) Ltd., New Delhi, pp 185–185 ISBN 9781620816493.
Pelicano H, Carney D, Huang P (2004) ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 7:97–110. https://doi.org/10.1016/j.drup.2004.01.004
Ciamporcero E, Daga M, Pizzimenti S, Roetto A, Dianzani C, Compagnone A, Palmieri A, Ullio C, Cangemi L, Pili R et al (2018) Crosstalk between Nrf2 and YAP contributes to maintaining the antioxidant potential and chemoresistance in bladder cancer. Free Radic Biol Med 115:447–457. https://doi.org/10.1016/j.freeradbiomed.2017.12.005
Trachootham D, Alexandre J, Huang P (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8:579–591. https://doi.org/10.1038/nrd2803
Taguchi K, Motohashi H, Yamamoto M (2011) Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16:123–140. https://doi.org/10.1111/j.1365-2443.2010.01473.x
Sun Y, Guan Z, Zhao W, Jiang Y, Li Q, Cheng Y, Xu Y (2017) Silibinin suppresses bladder cancer cell malignancy and chemoresistance in an NF-κB signal-dependent and signal-independent manner. Int J Oncol 51:1219–1226. https://doi.org/10.3892/ijo.2017.4089
Umemura A, He F, Taniguchi K, Nakagawa H, Yamachika S, Font-Burgada J, Zhong Z, Subramaniam S, Raghunandan S, Duran A et al (2016) p62, upregulated during preneoplasia, induces hepatocellular carcinogenesis by maintaining survival of stressed HCC-initiating cells. Cancer Cell 29:935–948. https://doi.org/10.1016/j.ccell.2016.04.006
Taniguchi K, Karin M (2018) NF-κB, inflammation, immunity and cancer: coming of age. Nat Rev Immunol 18:309–324. https://doi.org/10.1038/nri.2017.142
Ciamporcero E, Shen H, Ramakrishnan S, Yu KS, Chintala S, Shen L, Adelaiye R, Miles KM, Ullio C, Pizzimenti S et al (2016) YAP activation protects urothelial cell carcinoma from treatment-induced DNA damage. Oncogene 35:1541–1553. https://doi.org/10.1038/onc.2015.219
Yang X, Yin H, Zhang Y, Li X, Tong H, Zeng Y, Wang Q, He W (2018) Hypoxia-induced autophagy promotes gemcitabine resistance in human bladder cancer cells through hypoxia-inducible factor 1α activation. Int J Oncol 53:215–224. https://doi.org/10.3892/ijo.2018.4376
Haenisch S, Cascorbi I (2012) miRNAs as mediators of drug resistance. Epigenomics 4:369–381. https://doi.org/10.2217/epi.12.39
Deng H, Lv L, Li Y, Zhang C, Meng F, Pu Y, Xiao J, Qian L, Zhao W, Liu Q et al (2014) miR-193a-3p regulates the multi-drug resistance of bladder cancer by targeting the LOXL4 gene and the Oxidative Stress pathway. Mol Cancer 13:234. https://doi.org/10.1186/1476-4598-13-234
Giacomini I, Ragazzi E, Pasut G, Montopoli M (2020) The pentose phosphate pathway and its involvement in cisplatin resistance. Int J Mol Sci 21:937. https://doi.org/10.3390/ijms21030937
Gonenc A, Erten D, Aslan S, Akinci M, Simsek B, Torun M (2006) Lipid peroxidation and antioxidant status in blood and tissue of malignant breast tumor and benign breast disease. Cell Biol Int 30:376–380. https://doi.org/10.1016/j.cellbi.2006.02.005
Marikovsky M, Nevo N, Vadai E, Harris-Cerruti C (2002) Cu/Zn superoxide dismutase plays a role in angiogenesis. Int J Cancer 97:34–41. https://doi.org/10.1002/ijc.1565
Blaszczak W, Barczak W, Masternak J, Kopczyński P, Zhitkovich A, Rubiś B (2019) Vitamin C as a modulator of the response to cancer therapy. Molecules 24:453. https://doi.org/10.3390/molecules24030453
Klimant E, Wright H, Rubin D, Seely D, Markman M (2018) Intravenous vitamin C in the supportive care of cancer patients: a review and rational approach. Curr Oncol 25:139. https://doi.org/10.3747/co.25.3790
Yalçin O, Karataş F, Erulaş FA, Özdemir E (2004) The levels of glutathione peroxidase, vitamin A, E, C and lipid peroxidation in patients with transitional cell carcinoma of the bladder. BJU Int 93:863–866. https://doi.org/10.1111/j.1464-410X.2003.04729.x
Peh HY, Tan WSD, Liao W, Wong WSF (2016) Vitamin E therapy beyond cancer: tocopherol versus tocotrienol. Pharmacol Ther 162:152–169. https://doi.org/10.1016/j.pharmthera.2015.12.003
Jain A, Tiwari A, Verma A, Jain SK (2018) Vitamins for cancer prevention and treatment: an insight. Curr Mol Med. https://doi.org/10.2174/1566524018666171205113329
Zaidi SMKR, Al-Qirim TM, Banu N (2005) Effects of antioxidant vitamins on glutathione depletion and lipid peroxidation induced by restraint stress in the rat liver. Drugs R D 6:157–165. https://doi.org/10.2165/00126839-200506030-00004
Calaf GM, Aguayo F, Sergi CM, Juarranz A, Roy D (2018) Antioxidants and cancer: theories, techniques, and trials in preventing cancer. Oxid Med Cell Longev 2018:1–2. https://doi.org/10.1155/2018/5363064
Felsenstein KM, Theodorescu D (2018) Precision medicine for urothelial bladder cancer: update on tumour genomics and immunotherapy. Nat Rev Urol 15:92–111. https://doi.org/10.1038/nrurol.2017.179
Gorrini C, Harris IS, Mak TW (2013) Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov 12:931–947. https://doi.org/10.1038/nrd4002
Jones RG, Thompson CB (2009) Tumor suppressors and cell metabolism. Genes Dev 23:537–548. https://doi.org/10.1101/gad.1756509.GENES
Liu JM, Pan F, Li L, Liu QR, Chen Y, Xiong XX, Cheng K, Yu SB, Shi Z, Yu AC-H et al (2013) Piperlongumine selectively kills glioblastoma multiforme cells via reactive oxygen species accumulation dependent JNK and p38 activation. Biochem Biophys Res Commun 437:87–93. https://doi.org/10.1016/j.bbrc.2013.06.042
Liu D, Qiu XY, Wu X, Hu DX, Li CY, Yu SB, Pan F, Chen XQ (2017) Piperlongumine suppresses bladder cancer invasion via inhibiting epithelial mesenchymal transition and F-actin reorganization. Biochem Biophys Res Commun 494:165–172. https://doi.org/10.1016/j.bbrc.2017.10.061
Berger J, Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53:409–435. https://doi.org/10.1146/annurev.med.53.082901.104018
Wang G, Cao R, Wang Y, Qian G, Dan HC, Jiang W, Ju L, Wu M, Xiao Y, Wang X (2016) Simvastatin induces cell cycle arrest and inhibits proliferation of bladder cancer cells via PPARγ signalling pathway. Sci Rep 6:35783. https://doi.org/10.1038/srep35783
Cao R, Wang G, Qian K, Chen L, Ju L, Qian G, Wu C-L, Dan HC, Jiang W, Wu M et al (2018) TM4SF1 regulates apoptosis, cell cycle and ROS metabolism via the PPARγ-SIRT1 feedback loop in human bladder cancer cells. Cancer Lett 414:278–293. https://doi.org/10.1016/j.canlet.2017.11.015
Choudhary S, Rathore K, Wang H-CR (2011) Differential induction of reactive oxygen species through Erk1/2 and Nox-1 by FK228 for selective apoptosis of oncogenic H-Ras-expressing human urinary bladder cancer J82 cells. J Cancer Res Clin Oncol 137:471–480. https://doi.org/10.1007/s00432-010-0910-z
Choudhary S, Wang H-CR (2009) Role of reactive oxygen species in proapoptotic ability of oncogenic H-Ras to increase human bladder cancer cell susceptibility to histone deacetylase inhibitor for caspase induction. J Cancer Res Clin Oncol 135:1601–1613. https://doi.org/10.1007/s00432-009-0608-2
Wang H, Jiang D, Liu J, Ye S, Xiao S, Wang W, Sun Z, Xie Y, Wang J (2013) Compound K induces apoptosis of bladder cancer T24 cells via reactive oxygen species-mediated p38 MAPK pathway. Cancer Biother Radiopharm 28:607–614. https://doi.org/10.1089/cbr.2012.1468
Duan F, Yu Y, Guan R, Xu Z, Liang H, Hong L (2016) Vitamin K2 induces mitochondria-related apoptosis in human bladder cancer cells via ROS and JNK/p38 MAPK signal pathways. PLoS ONE 11:e0161886. https://doi.org/10.1371/journal.pone.0161886
Zeng J, Sun Y, Wu K, Li L, Zhang G, Yang Z, Wang Z, Zhang D, Xue Y, Chen Y et al (2011) Chemopreventive and chemotherapeutic effects of intravesical silibinin against bladder cancer by acting on mitochondria. Mol Cancer Ther 10:104–116. https://doi.org/10.1158/1535-7163.MCT-10-0577
Zhuo Z, Song Z, Ma Z, Zhang Y, Xu G, Chen G (2019) Chlorophyllin e6-mediated photodynamic therapy inhibits proliferation and induces apoptosis in human bladder cancer cells. Oncol Rep 41:2181–2193. https://doi.org/10.3892/or.2019.7013
Yan D, Sherman JH, Keidar M (2017) Cold atmospheric plasma, a novel promising anti-cancer treatment modality. Oncotarget 8:15977–15995. https://doi.org/10.18632/oncotarget.13304
Semmler ML, Bekeschus S, Schäfer M, Bernhardt T, Fischer T, Witzke K, Seebauer C, Rebl H, Grambow E, Vollmar B et al (2020) Molecular mechanisms of the efficacy of cold atmospheric pressure plasma (CAP) in cancer treatment. Cancers (Basel) 12:269. https://doi.org/10.3390/cancers12020269
Yan D, Talbot A, Nourmohammadi N, Sherman JH, Cheng X, Keidar M (2015) Toward understanding the selective anticancer capacity of cold atmospheric plasma—a model based on aquaporins (Review). Biointerphases 10:040801. https://doi.org/10.1116/1.4938020
Braný D, Dvorská D, Halašová E, Škovierová H (2020) Cold atmospheric plasma: a powerful tool for modern medicine. Int J Mol Sci 21:2932. https://doi.org/10.3390/ijms21082932
Adachi T, Tanaka H, Nonomura S, Hara H, Kondo S, Hori M (2015) Plasma-activated medium induces A549 cell injury via a spiral apoptotic cascade involving the mitochondrial–nuclear network. Free Radic Biol Med 79:28–44. https://doi.org/10.1016/j.freeradbiomed.2014.11.014
Xiang L, Xu X, Zhang S, Cai D, Dai X (2018) Cold atmospheric plasma conveys selectivity on triple negative breast cancer cells both in vitro and in vivo. Free Radic Biol Med 124:205–213. https://doi.org/10.1016/j.freeradbiomed.2018.06.001
Chen Z, Simonyan H, Cheng X, Gjika E, Lin L, Canady J, Sherman J, Young C, Keidar M (2017) A novel micro cold atmospheric plasma device for glioblastoma both in vitro and in vivo. Cancers (Basel) 9:61. https://doi.org/10.3390/cancers9060061
Babington P, Rajjoub K, Canady J, Siu A, Keidar M, Sherman JH (2015) Use of cold atmospheric plasma in the treatment of cancer. Biointerphases 10:029403. https://doi.org/10.1116/1.4915264
Boehm D, Bourke P (2018) Safety implications of plasma-induced effects in living cells—a review of in vitro and in vivo findings. Biol Chem 400:3–17. https://doi.org/10.1515/hsz-2018-0222
Tavares-da-Silva E, Pereira E, Pires AS, Neves AR, Braz-Guilherme C, Marques IA, Abrantes AM, Gonçalves AC, Caramelo F, Silva-Teixeira R et al (2021) Cold atmospheric plasma, a novel approach against bladder cancer, with higher sensitivity for the high-grade cell line. Biology (Basel) 10:41. https://doi.org/10.3390/biology10010041
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This research was funded by the National Funds via Foundation for Science and Technology (FCT), Portugal through Strategic Projects UID/NEU/04539/2019,UIDB/04539/2020 and UIDP/04539/2020 (CIBB), by the Fellowship SFRH/BD/ 136973/2018 from FCT, and by the “Bolsa de Investigação JABA RECORDATI Urologia 2017”.
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Conceptualization, FM, DM, AMA and MFB; methodology, ETS, AF, ASP and EP; writing review draft preparation, FM, DM, ETS, ASP and EP; writing—review and editing, FM, DM, AMA, ETS, EP, AF and MFB; supervision, FM, DM and MFB; funding acquisition, FM, ETS, AMA and AF.
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Mendes, F., Pereira, E., Martins, D. et al. Oxidative stress in bladder cancer: an ally or an enemy?. Mol Biol Rep 48, 2791–2802 (2021). https://doi.org/10.1007/s11033-021-06266-4
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DOI: https://doi.org/10.1007/s11033-021-06266-4