A mini-review of reactive oxygen species in urological cancer: Correlation with NADPH oxidases, angiogenesis, and apoptosis

International Journal of Molecular Sciences

Volumn 18, Issue 10, 2017, Pages

  Miyata, Yasuyoshi ^a   Matsuo, Tomohiro ^a   Sagara, Yuji ^a   Ohba, Kojiro ^a   Ohyama, Kaname ^a   Sakai, Hideki ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

Author keywords

Angiogenesis; Apoptosis; NADPH oxidases; Reactive oxygen species; Urological cancers

Indexed keywords

ARSENIC TRIOXIDE; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VANADIC ACID;

ANGIOGENESIS; APOPTOSIS; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CHROMOSOMAL INSTABILITY; CORRELATIONAL STUDY; DRUG THERAPY; GENE EXPRESSION; GENE MUTATION; GLEASON SCORE; HUMAN; METASTASIS; NONHUMAN; OXIDATIVE STRESS; PROSTATE CANCER; RENAL CELL CARCINOMA; REVIEW; SOLID MALIGNANT NEOPLASM; TUMOR GROWTH; URINARY TRACT CANCER; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; URINARY TRACT TUMOR;

APOPTOSIS; CARCINOGENESIS; HUMANS; NADPH OXIDASES; NEOVASCULARIZATION, PATHOLOGIC; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; UROLOGIC NEOPLASMS;

EID: 85031994297     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18102214     Document Type: Review

References (161)

1. Sies, H. Oxidative stress: Oxidants and antioxidants. Exp. Physiol. 1997, 82, 291-295.
2. Goodman, M.; Bostick, R.M.; Dash, C.; Terry, P.; Flanders, W.D.; Mandel, J. A summary measure of proand anti-oxidant exposures and risk of incident, sporadic, colorectal adenomas. Cancer Causes Control 2008, 19, 1051-1064.
3. Pizzino, G.; Irrera, N.; Cucinotta, M.; Pallio, G.; Mannino, F.; Arcoraci, V.; Squadrito, F.; Altavilla, D.; Bitto, A. Oxidative Stress: Harms and Benefits for Human Health. Oxid. Med. Cell. Longev. 2017, 2017, 8416763.
4. Andrisic, L.; Dudzik, D.; Barbas, C.; Milkovic, L.; Grune, T.; Zarkovic, N. Short overview on metabolomics approach to study pathophysiology of oxidative stress in cancer. Redox Biol. 2017, 14, 47-58.
5. Carini, F.; Mazzola, M.; Rappa, F.; Jurjus, A.; Geagea, A.G.; Al Kattar, S.; Bou-Assi, T.; Jurjus, R.; Damiani, P.; Leone, A.; et al. Colorectal carcinogenesis: Role of oxidative stress and antioxidants. Anticancer Res. 2017, 37, 4759-4766.
6. Schieber, M.; Chandel, N.S. ROS function in redox signaling and oxidative stress. Curr. Biol. 2014, 24, R453-462.
7. D’Autréaux, B.; Toledano, M.B. ROS as signaling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 2007, 8, 813-824.
8. Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39, 44-84.
9. Halliwell, B. The antioxidant paradox: Less paradoxical now? Br. J. Clin. Pharmacol. 2013, 75, 637-644.
10. Brown, D.I.; Griendling, K.K. Regulation of signal transduction by reactive oxygen species in the cardiovascular system. Circ. Res. 2015, 116, 531-549.
11. Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov. 2009, 8, 579-591.
12. Du, M.Q.; Carmichael, P.I.; Phillips, D.H. Induction of activating mutations in the human c-Ha-ras-a protooncogene by oxygen free radicals. Mol. Carcinog. 1994, 11, 170-175.
13. Ushijima, T. detection and interpretation of altered methylation patterns in cancer cells. Nat. Rev. Cancer. 2005, 5, 223-231.
14. Toyokuni, S. Molecular mechanisms of oxidative stress-induced carcinogenesis: From epidemiology to oxygenomics. IUBMB Life 2008, 60, 441-447.
15. Lee, K.H.; Kim, S.W.; Kim, J.R. Reactive oxygen species regulate urokinase plasminogen activator expression and cell invasion via mitogen-activated protein kinase pathways after treatment with hepatocyte growth factor in stomach cancer cells. J. Exp. Clin. Cancer Res. 2009, 28, 73.
16. Liou, G.Y.; Storz, P. Reactive oxygen species in cancer. Free Radic. Res. 2010, 44, 479-496.
17. Li, Q.; Engelhardt, J.F. Interleukin-1β induction of NFκB is partially regulated by H2O2-mediated activation of NFκB-inducing kinase. J. Biol. Chem. 2006, 281, 1495-1505.
18. Fresno Vara, J.A.; Casado, E.; de Castro, J.; Cejas, P.; Belda-Iniesta, C.; González-Barón, M. PI3K/Akt signaling pathway and cancer. Cancer Treat. Rev. 2004, 30, 193-204.
19. Kwon, J.; Lee, S.R.; Yang, K.S.; Ahn, Y.; Kim, Y.J.; Stadtman, E.R.; Rhee, S.G. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factor. Proc. Natl. Acad. Sci. USA 2004, 101, 16419-16424.
20. Saybasilli, H.; Yülsel, M.; Haklar, G.; Yalçin A.S. Effect of mitochondrial electron transport chain inhibitors on superoxide radical generation in rat hippocampal and striatal slices. Antioxid. Redox Signal. 2001, 3, 1099-1104.
21. Li, X.; Fang, P.; Mai, J.; Choi, E.T.; Wang, H.; Yang, X.F. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 2013, 6, 19.
22. Segal, A.W.; Shatwell, K.P. The NAPDH oxidase of phagocytic leukemia. Ann. N. Y. Acad. Sci. 1997, 832, 215-222.
23. Kröller-Schön, S.; Steven, S.; Kossmann, S.; Scholz, A.; Daub, S.; Oelze, M.; Xia, N.; Hausding, M.; Mikhed, Y.; Zinssius, E.; et al. Molecular mechanisms of the crosstalk between mitochondria and NADPH oxidase through reactive oxygen species-studies in white blood cells and in animal models. Antioxid. Redox Signal. 2015, 20, 247-266.
24. Korbecki, J.; Baranowska-Bosiacka, I.; Gutowska, I.; Chlubek, D. The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. J. Physiol. Pharmacol. 2013, 64, 409-421.
25. Nelson, K.K.; Melendez, J.A. Mitochondrial redox control of matrix metalloproteinases. Free Radic. Biol. Med. 2004, 37, 768-784.
26. Siwik, D.A.; Colucci, W.S. Regulation of matrix metalloproteinases by cytokines and reactive oxygen/nitrogen species in the myocardium. Heart Fail. Rev. 2004, 9, 43-51.
27. Fiaschi, T.; Cozzi, G.; Raugei, G.; Formigli, L.; Ramponi, G.; Chiarugi, P. Redox regulation of β-actin during integrin-mediated cell adhesion. J. Biol. Chem. 2006, 281, 22983-22991.
28. Galadari, S.; Rahman, A.; Pallichankandy, S.; Thayyullathil, F. Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radic. Biol. Med. 2017, 104, 144-164.
29. Leufkens, A.M.; van Duijnhoven, F.J.; Woudt, S.H.; Siersema, P.D.; Jenab, M.; Jansen, E.H.; Pischon, T.; Tjønneland, A.; Olsen, A.; Overvad, K.; et al. Biomarkers of oxidative stress and risk of developing colorectal cancer: A cohort-nested case-control study in the European Prospective Investigation Into Cancer and Nutrition. Am. J. Epidemiol. 2012, 175, 653-663.
30. Tochhawng, L.; Deng, S.; Pervaiz, S.; Yap, C.T. Redox regulation of cancer cell migration and invasion. Mitochondrion 2013, 13, 246-253.
31. Prasad, S.; Gupta, S.C.; Tyagi, A.K. Reactive oxygen species (ROS) and cancer: Role of antioxidative nutraceuticals. Cancer Lett. 2017, 387, 95-105.
32. Toyokuni, S.; Okamoto, K.; Yodoi, J.; Hiai, H. Persistent oxidative stress in cancer. FEBS Lett. 1995, 358, 1-3.
33. Schumacker, P.T. Reactive oxygen species in cancer: A dance with the devil. Cancer Cell. 2015, 27, 156-157.
34. Morry, J.; Ngamcherdtrakul, W.; Yantasee, W. Oxidative stress in cancer and fibrosis: Opportunity for therapeutic intervention with antioxidant compounds, enzymes, and nanoparticles. Redox Biol. 2017, 11, 240-253.
35. Szatrowski, T.P.; Nathan, C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51, 794-798.
36. Panieri, E.; Santoro, M.M. ROS homeostasis and metabolism: A dangerous liason in cancer cells. Cell Death Dis. 2016, 7, e2253.
37. Lambeth, J.D.; Kawahara, T.; Diebold, B. Regulation of Nox and Duox enzymatic activity and expression. Free Radic. Biol. Med. 2007, 43, 319-331.
38. Jiang, F.; Zhang, Y.; Dusting, G.J. NADPH oxidase-mediated redox signaling: Roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol. Rev. 2011, 63, 218-242.
39. Gào, X.; Schöttker, B. Reduction-oxidation pathways involved in cancer development: A systematic review of literature reviews. Oncotarget 2017, 8, 51888-51906.
40. Block, K.; Gorin, Y. Aiding and abetting roles of NOX oxidases in cellular transformation. Nat. Rev. Cancer 2012, 12, 627-637.
41. Suh, Y.A.; Arnold, R.S.; Lassegue, B.; Shi, J.; Xu, X.; Sorescu, D.; Chung, A.B.; Griendling, K.K.; Lambeth, J.D. Cell transformation by the superoxide-generating oxidase MOX1. Nature 1999, 13, 16-22.
42. Arnold, R.S.; Shi, J.; Murad, E.; Whalen, A.M.; Sun, C.Q.; Polavarapu, R.; Parthasarathy, S.; Petros, J.A.; Lambeth, J.D. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci. USA 2001, 98, 5550-5555.
43. Böhm, B.; Heinzelmann, S.; Motz, M.; Bauer, G. Extracellular localization of catalase is associated with the transformed state of malignant cells. Biol. Chem. 2015, 396, 1339-1356.
44. Heinzelmann, S.; Bauer, G. Multiple protective functions of catalase against intercellular apoptosis inducing ROS signaling of human tumor cells. Biol. Chem. 2010, 391, 675-693.
45. Bauer, G. Increasing the endogenous NO level causes catalase inactivation and reactivation of intercellular apoptosis signaling specifically in tumor cells. Redox Biol. 2015, 6, 353-371.
46. Bánfi, B.; Muturana, A.; Jaconi, S.; Arnaudeau, S.; Laforge, T.; Sinha, B.; Ligeti, E.; Demaurex, N.; Krause K.H. A mammalian H+ channel generated trough alternative splicing of the NADPH oxidase homolog NOH-1. Science 2000, 287, 138-142.
47. Kobayashi, S.; Nojima, Y.; Shibuya, M.; Maru, Y. Nox1 regulates apoptosis and potentially stimulates branching morphogenesis in sinusoidal endothelial cells. Exp. Cell Res. 2004, 300, 455-462.
48. Shinihara, M.; Shang, W.H.; Kubodera, M.; Harada, S.; Mitsushita, J.; Kato, M.; Miyazaki, H.; Sumimoto, H.; Kamata, T. Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesion by down-regulating Rho. J. Biol. Chem. 2007, 282, 17640-17648.
49. Shimada, K.; Nakamura, M.; Anai, S.; De Velasco, M.; Tanaka, M.; Tsujikawa, K.; Ouji, Y.; Konishi, N. A novel human AlkB homologue, ALKBH8, contributes to human bladder cancer progression. Cancer Res. 2009, 69, 3157-3164.
50. De Carvalbo, D.D.; Sadok, A.; Bourgarel-Rey, V.; Gattacceca, F.; Penel, C.; Lehmann, M.; Kovacic, H. Nox1 downstream of 12-lipoxygenase controls cell proliferation but not cell spreading of colon cancer. Int. J. Cancer 2008, 122, 1757-1764.
51. Raad, H.; Serrano-Sanchez, M.; Harfouche, G.; Mahfouf, W.; Bortolotto, D.; Bergeron, V.; Kasraian, Z.; Dousset, L.; Hosseini, M.; Taieb, A.; et al. NADPH oxidase-1 plays a key role in keratinocyte responses to UV radiation and UVB-induced skin carcinogenesis. J. Investig. Dermatol. 2017, 137, 1311-1321.
52. Bhardwaj, V.; Gokulan, R.C.; Horvat, A.; Yermalitskaya, L.; Korolkova, O.; Washington, K.M.; El-Rifai, W.; Dikalov, S.I. Zaika, A.I. Activation of NADPH oxidases leads to DNA damage in esophageal cells. Sci. Rep. 2017, 7, 9956.
53. Aydin, E.; Johansson, J.; Nazir, F.H.; Hellstrand, K.; Martner, A. Role of NOX2-derived reactive oxygen species in NK cell-mediated control of murine melanoma metastasis. Cancer Immunol. Res. 2017, 5, 804-811.
54. Aurelius, J.; Hallner, A.; Werlenius, O.; Riise, R.; Möllgård, L.; Brune, M.; Hansson, M.; Martner, A.; Thorén, F.B.; Hellstrand, K. NOX2-dependent immunosuppression in chronic myelomonocytic leukemia. J. Leukoc. Biol. 2017, 102, 459-466.
55. Montalvo-Javé, E.E.; Olguín-Martínez, M.; Hernández-Espinosa, D.R.; Sánchez-Sevilla, L.; Mendieta- Condado, E.; Contreras-Zentella, M.L.; Oñate-Ocaña, L.F.; Escalante-Tatersfield, T.; Echegaray-Donde, A.; Ruiz-Molina, J.M.; et al. Role of NADPH oxidases in inducing a selective increase of oxidant stress and cyclin D1 and checkpoint 1 over-expression during progression to human gastric adenocarcinoma. Eur. J. Cancer. 2016, 57, 50-57.
56. Bánfi, B.; Malgrange, B.; Knisz, J.; Steger, K.; Steger, K.; Dubois-Dauphin, M.; Krause, K.H. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 2004, 279, 46065-46072.
57. Wang, Y.; Liu, Q.; Zhao, W.; Zhou, X.; Miao, G.; Sun, C.; Zhang, H. NADPH oxidase activation contributes to heavy ion irradiation-induced cell death. Dose Response 2017, 15, 1559325817699697
58. Leung, E.L.; Fan, X.X.; Wong, M.P.; Jiang, Z.H.; Liu, Z.Q.; Yao, X.J.; Lu, L.L.; Zhou, Y.L.; Yau, L.F.; Tin, V.P.; et al. Targeting tyrosine kinase inhibitor-resistant non-small cell lung cancer by inducing epidermal growth factor receptor degradation via methionine 790 oxidation. Antioxid. Redox Signal. 2016, 24, 263-279.
59. Cheng, G.; Cao, Z.; Xu, X.; van Meir, E.G.; Lambeth, J.D. Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 2001, 269, 131-140.
60. Lee, J.K.; Edderkaoui, M.; Truong, P.; Ohno, I.; Jang, K.T.; Berti, A.; Pandol, S.J.; Gukovskaya, A.S. NADPH oxidase promotes pancreatic cancer cell survival via inhibiting JAK2 dephosphorylation by tyrosine phosphatases. Gastroenterology 2007, 133, 1637-1648.
61. Maloney, E.; Sweet, I.R.; Hockenbery, D.M.; Pharm M.; Rizzo, N.O.; Tateya, S.; Handa, P.; Schwartz, M.W.; Kim, F. Activation of NF-κB by palmitate in endothelial cells, a key role for NADPH oxidase-derived superoxide in response to TLR4. Activation 2009, 29, 1370-1375.
62. Liu, R.-M.; Choi, J.; Wu, J.-H.; Gaston Pravia, K.A.; Lewis, K.M.; Brand, J.D.; Mochel, N.S.; Krzywanski, D.M.; Lambeth, J.D.; Hagood, J.S.; et al.; Postlethwait EM. Oxidative modification of nuclear mitogenactivated protein kinase phosphatase 1 is involved in transforming growth factor β1-induced expression of plasminogen activator inhibitor 1 in fibroblasts. J. Biol. Chem. 2010, 285, 16239-16247.
63. Brar, S.S.; Kennedy, T.P.; Whorton, A.R.; Sturrock, A.B.; Huecksteadt, T.P.; Ghio, A.J.; Hoidal, J.R. Reactive oxygen species from NAD(P)H: Quinone oxidoreductase constitutively activate NF-κB in malignant melanoma cells. Am. J. Physiol. 2001, 280, C659-C369.
64. Vaquero, E.C.; Edderkaoui, M.; Pandol, S.; Gukovsky, I.; Gukovskaya, A.S. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J. Biol. Chem. 2004, 279, 34643-34654.
65. Xia, C.; Meng, Q.; Liu, L.Z.; Rojanasakul, Y.; Wang, X.R.; Jiang, B.H. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 2007, 67, 10823-10830.
66. Datla, S.R.; Peshavariya, H; Dusting, G.J.; Mahadev, K.; Goldstein, B.J.; Jiang, F. Important role of Nox4 type NADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitro. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 2319-2324.
67. Vallet, P.; Charnay, Y.; Steger, K.; Ogier-Denis, E.; Kovari, E.; Herrmann, F.; Michel, J.P.; Szanto, I. Neuronal expression of the NADPH oxidase NOX4, and its regulation in mouse experimental brain ischemia. Neuroscience 2005, 132, 233-238.
68. Juhasz, A.; Ge, Y.; Markel, S.; Chiu, A.; Matsumoto, L.; Van, B.J.; Roy, K.; Doroshow, J.H. Expression of NADPH oxidase homologues and accessory genes in human cancer cell lines, tumours and adjacent normal tissues. Free Radic. Res. 2009, 43, 523-532.
69. Si, J.; Fu, X.; Behar, J.; Wands, J.; Beer, D.G.; Souza, R.F.; Spechler, S.J.; Lambeth, D.; Cao, W. NADPH oxidase NOX5-S mediates acid-induced cyclooxygenase-2 expression via activation of NF-κB in Barrett’s esophageal adenocarcinoma cells. J. Biol. Chem. 2007, 282, 16244-16255.
70. Ushio-Fukai, M.; Nakamura, Y. Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 2008, 266, 37-52.
71. Luxen, S.; Belinsky, S.A.; Knaus, U.G. Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res. 2008, 68, 1037-1045.
72. Chen, S.; Ling, Q.; Yu, K.; Huang, C.; Li, N.; Zheng, J.; Bao, S.; Cheng, Q.; Zhu, M.; Chen, M. Dual oxidase 1: A predictive tool for the prognosis of hepatocellular carcinoma patients. Oncol. Rep. 2016, 35, 3198-3208.
73. Little, A.C.; Sulovari, A.; Danyal, K.; Heppner, D.E.; Seward, D.J.; van der Vliet, A. Paradoxical roles of dual oxidases in cancer biology. Free Radic. Biol. Med. 2017, 110, 117-132.
74. Chen, S.S.; Yu, K.K.; Ling, Q.X.; Huang, C.; Li, N.; Zheng, J.M.; Bao, S.X.; Cheng, Q.; Zhu, M.Q.; Chen, M.Q. The combination of three molecular markers can be a valuable predictive tool for the prognosis of hepatocellular carcinoma patients. Sci. Rep. 2016, 6, 24582.
75. Wu, Y.; Antony, S.; Hewitt, S.M.; Jiang, G.; Yang, S.X.; Meitzler, J.L.; Juhasz, A.; Lu, J.; Liu, H.; Doroshow, J.H.; Roy, K. Functional activity and tumor-specific expression of dual oxidase 2 in pancreatic cancer cells and human malignancies characterized with a novel monoclonal antibody. Int. J. Oncol. 2013, 42, 1229-1238.
76. Qi, R.; Zhou, Y.; Li, X.; Guo, H.; Gao, L.; Wu, L.; Wang, Y.; Gao, Q. DUOX2 expression is increased in Barrett esophagus and cancerous tissues of stomach and colon. Gastroenterol. Res. Pract. 2016, 2016, 1835684.
77. Brar, S.S.; Corbib, Z.; Kennedy, T.P.; Hemendinger, R.; Thornton, L.; Bommarius, B.; Arnold, R.S.; Whorton, A.R.; Sturrock, A.B.; Huecksteadt, T.P.; et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU145 prostate cancer cells. Am. J. Physiol. Cell Physiol. 2003, 285, C353-C369.
78. Kumar, B.; Koul, S.; Khandrika, L.; Meacham, R.B.; Koul, H.K. Oxidative stress in inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 2008, 68, 1777-1785.
79. Höll, M.; Koziel, R.; Schäfer, G.; Pircher, H.; Pauck, A.; Hermann, M.; Klocker, H.; Jansen-Dürr, P.; Sampson, N. ROS signaling by NADPH oxidase 5 modulates the proliferation and survival of prostate carcinoma cells. Mol. Carcinog. 2016, 55, 27-39.
80. Arbiser, J.L.; Petros, J.; Klafter, R.; Govindajaran, B.; McLaughlin, E.R.; Brown, L.F.; Cohen, C.; Moses, M.; Kilroy, S.; Arnold, R.S.; et al. Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc. Natl. Acad. Sci. USA 2001, 99, 715-720.
81. Lim, S.D.; Sun, C.Q.; Lambeth, J.D.; Marshall, F.; Amin, M.; Chung, L.; Petros, J.A.; Arnold, R.S. Increased Nox1 and hydrogen peroxide in prostate cancer. Prostate 2005, 62, 200-207.
82. Deep, G.; Kumar, R.; Jain, A.K.; Dhar, D.; Panigrahi, G.K.; Hussain, A.; Agarwal, C.; El-Elimat, T.; Sica, V.P.; Oberlies, N.H.; et al. Graviola inhibits hypoxia-induced NADPH oxidase activity in prostate cancer cells reducing their proliferation and clonogenicity. Sci. Rep. 2016, 6, 23135.
83. Tamura, R.E.; Hunger, A.; Fernandes, D.C.; Laurindo, F.R.; Costanzi-Strauss, E.; Strauss, B.E. Induction of oxidants distinguishes susceptibility of prostate carcinoma cell lines to p53 gene transfer mediated by an improved adenoviral vector. Hum. Gene Ther. 2017, 28, 639-653.
84. Arnold, R.S.; He, J.; Remo, A.; Ritsick, D.; Yin-Goen, Q.; Lambeth, J.D.; Datta, M.W.; Young, A.N.; Petros, J.A. Nox1 expression determines cellular reactive oxygen and modulates c-fos-induced growth factor, interleukin-8 and cav-1. Am. J. Pahol. 2007, 171, 2021-2032.
85. Pettigrew, C.A.; Clerkin, J.S.; Cotter, T.G. DUOX enzyme activity promotes AKT signalling in prostate cancer cells. Anticancer Res. 2012, 32, 5175-5181.
86. Tam, N.; Gao, Y.; Leung, Y.; Ho, S.M.; Androgenic regulation of oxidative stress in the rat prostate: Involvement of NAD(P)H oxidase and antioxidant defense machinery during prostatic involution and regrowth. Am. J. Pathol. 2003, 163, 2513-2522.
87. Lu, J.P.; Monardo, L.; Bryskin, I.; Hou, Z.F.; Trachtenberg, J.; Wilson, B.C.; Pinthus, J.H. Androgens induce oxidative stress and radiation resistance in prostate cancer cells though NADPH oxidase. Prostate Cancer Prostatic Dis. 2010, 13, 39-46.
88. Lu, J.P.; Hou, Z.F.; Duivenvoorden, W.C.; Whelan, K.; Honig, A.; Pinthus, J.H. Adiponectin inhibits oxidative stress in human prostate carcinoma cells. Prostate Cancer Prostatic Dis. 2012, 15, 28-35.
89. Antony, S.; Wu, Y.; Hewitt, S.M.; Anver, M.R.; Butcher, D.; Jiang, G.; Meitzler, J.L.; Liu, H.; Juhasz, A.; Lu, J.; et al. Characterization of NADPH oxidase 5 expression in human tumors and tumor cell lines with a novel mouse monoclonal antibody. Free Radic. Biol. Med. 2013, 65, 497-508.
90. Huang, W.C.; Li, X.; Liu, J.; Lin, J.; Chung, L.W. Activation of androgen receptor, lipogenesis, and oxidative stress converged by SREBP-1 is responsible for regulating growth and progression of prostate cancer cells. Mol. Cancer Res. 2012, 10, 133-142.
91. Block, K.; Gorin, Y.; Hoover, P.; Williams, P.; Chelmicki, T.; Clark, R.A.; Yoneda, T.; Abboud, H.E. NAD(P)H oxidases regulate HIF-2α protein expression. J. Biol. Chem. 2007, 282, 8019-8026.
92. Gregg, J.L.; Turner, R.M.; 2nd.; Chang, G.; Joshi, D.; Zhan, Y.; Chen, L.; Maranchie, J.K. NADPH oxidase NOX4 supports renal tumorigenesis by promoting the expression and nuclear accumulation of HIF2α. Cancer Res. 2014, 74, 3501-3511.
93. Chang, G.; Chen, L.; Lin, H.M.; Lin, Y.; Maranchie, J.K. Nox4 inhibition enhances the cytotoxicity of cisplatin in human renal cancer cells. J. Exp. Ther. Oncol. 2012, 10, 9-18.
94. Shanmugasundaram, K.; Block, K. Renal carcinogenesis, tumor heterogeneity, and reactive oxygen species: Tactics evolved. Antioxid. Redox Signal. 2016, 25, 685-701.
95. Tsujikawa, K.; Koike, K.; Kitae, K.; Shinkawa, A.; Arima, H.; Suzuki, T.; Tsuchiya, M.; Makino, Y.; Furukawa, T.; Konishi, N.; et al. Expression and sub-cellular localization of human ABH family molecules. J. Cell Mol. Med. 2007, 11, 1105-1116.
96. Choudhary, S.; Rathore, K.; Wang, H.C. Differential induction of reactive oxygen species through Erk1/1 and Nox-1 by FK228 for selective apoptosis of oncogenic H-Ras-expressing human urinary bladder cancer J82 cells. J. Cancer Res. Clin. Oncol. 2011, 137, 471-480.
97. Shimada, K.; Fujii, T.; Tsujikawa, K.; Anai, S.; Fujimoto, K.; Konishi, N. ALKBH3 contributes to survival and angiogenesis of human urothelial carcinoma cells through NADPH oxidase and Tweak/Fn14/VEGF signals. Clin. Cancer Res. 2012, 18, 5247-5255.
98. Shimada, K.; Fujii, T.; Anai, S. ROS generation via NOX4 and its utility in the cytological diagnosis of urothelial carcinoma of the urinary bladder. BMC Cancer 2011, 11, 22.
99. Kim, E.Y.; Seo, J.M.; Kim, C.; Lee, J.E.; Lee, K.M.; Kim, J.H. BLT2 promotes the invasion and metastasis of aggressive bladder cancer cells through a reactive oxygen species-linked pathway. Free Radic. Biol. Med. 2010, 49, 1072-1081.
100. Matsuo, T.; Miyata, Y.; Asai, A.; Sagara, Y.; Furusato, B.; Fukuoka, J.; Sakai, H. Green tea polyphenol induces changes in cancer-related factors in an animal model of bladder cancer. PLoS ONE 2017, 12, e0171091.
101. Miyata, Y.; Mitsunari, K.; Asai, A.; Takehara, K.; Mochizuki, Y.; Sakai, H. Pathological significance and prognostic role of microvessel density, evaluated using CD31, CD34, and CD105 in prostate cancer patients after radical prostatectomy with neoadjuvant therapy. Prostate 2015, 75, 84-91.
102. Abid, M.R.; Spokes, S.C.; Shih, W.C.; Aird, W.C. NAPDH oxidase activity selectively modulates vascular endothelial growth factor signaling pathway. J. Biol. Chem. 2007, 282, 35373-35385.
103. Kilmova, T.; Chandel, N.S. Mitochondrial complex III regulates hypoxic activation of HIF. Cell Death Differ. 2008, 15, 660-666.
104. Jing, Y.; Liu, L.Z.; Jiang, Y, Zhu, Y.; Guo, N.L.; Barnett, J.; Rojanasakul, Y.; Agani, F.; Jiang, B.H. Cadmium increases HIF-1 and VEGF expression through ROS, ERK, and Akt signaling pathways and induces malignant transformation of human bronchial epithelial cells. Toxicol. Sci. 2012, 125, 10-19.
105. Gao, N.; Ding, M.; Zheng, J.Z.; Zhang, Z.; Leonard, S.S.; Liu, K.J.; Shi, X.; Jiang, B.H. Vanadate-induced expression of hypoxia-inducible factor 1 alpha and vascular endothelial growth factor through phosphatidylinositol 3-kinase/Akt pathway and reactive oxygen species. J. Biol. Chem. 2002, 277, 31963-31971.
106. Turcotte, S.; Desrosiers, R.R.; Béliveau, R. HIF-1α mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J. Cell Sci. 2003, 116, 2247-2260.
107. Shin, D.H.; Dier, U.; Melendez, J.A.; Hempel, N. Regulation of MMP-1 expression in response to hypoxia is dependent on the intracellular redox status of metastatic bladder cancer cells. Biochim. Biophys. Acta 2015, 1852, 2593-2602.
108. Coso, S.; Harrison, I.; Harrison, C.B.; Vinh, A.; Sobey, C.G.; Drummond, G.R.; Williams, E.D.; Selemidis, S. NADPH oxidases as regulators of tumor angiogenesis: Current and emerging concepts. Antioxid. Redox Signal. 2012, 16, 1229-1247.
109. Prieto-Bermejo, R.; Hernández-Hernández, A. The Importance of NADPH Oxidases and Redox Signaling in Angiogenesis. Antioxidants (Basel) 2017, 6, E32.
110. Gao, N.; Shen, L.; Zhang, Z.; Leonard, S.S.; He, H.; Zhang, X.G.; Shi, X.; Jiang, B.H. Arsenite induces HIF- 1α and VEGF through PI3K, Akt and reactive oxygen species in DU145 human prostate carcinoma cells. Mol. Cell. Biochem. 2004, 255, 33-45.
111. Kou, X.; Fan, J.; Chen, N. Potential molecular targets of ampelopsin in prevention and treatment of cancers. Anticancer Agents Med. Chem. 2017, doi:10.2174/1871521409666170412130529.
112. Zhang, M.; Liu, C.; Zhang, Z.; Yang, S.; Zhang, B.; Yin, L.; Swarts, S.; Vidyasagar, S.; Zhang, L.; Okunieff, P. A new flavonoid regulates angiogenesis and reactive oxygen species production. Adv. Exp. Med. Biol. 2014, 812, 149-155.
113. Delle, M.S.; Sanità, P.; Calgani, A.; Schenone, S.; Botta, L.; Angelucci, A. Src inhibition potentiates antitumoral effect of paclitaxel by blocking tumor-induced angiogenesis. Exp. Cell Res. 2014, 328, 20-31.
114. Wu, C.T.; Chen, M.F.; Chen, W.C.; Hsieh, C.C. The role of IL-6 in the radiation response of prostate cancer. Radiat. Oncol. 2013, 8, 159.
115. Alcayaga-Miranda, F.; González, P.; Lopez-Verrilli, A.; Varas-Godoy, M.; Aguila-Diaz, C.; Contreras, L.; Khoury, M. Prostate tumor-induced angiogenesis is blocked by exosomes derived from menstrual stem cells through the inhibition of reactive oxygen species. Oncotarget 2016, 7, 44462-44477.
116. Golovine, K.; Makhov, P.; Naito, S.; Raiyani, H.; Tomaszewski, J.; Mehrazin, R.; Tulin, A.; Kutikov, A.; Uzzo, R.G.; Kolenko, V.M. Piperlongumine and its analogs down-regulate expression of c-Met in renal cell carcinoma. Cancer Biol. Ther. 2015, 16, 743-739.
117. Li, W.; Liu, M.; Xu, Y.F.; Feng, Y.; Che, J.P.; Wang, G.C.; Zheng, J.H. Combination of quercetin and hyperoside has anticancer effects on renal cancer cells through inhibition of oncogenic microRNA-27a. Oncol. Rep. 2014, 31, 117-124.
118. Tanaka, N.; Miyajima, A.; Kosaka, T.; Shirotake, S.; Hasegawa, M.; Kikuchi, E.; Oya, M. Cisdichlorodiammineplatinum upregulates angiotensin II type 1 receptors through reactive oxygen species generation and enhances VEGF production in bladder cancer. Mol. Cancer Ther. 2010, 9, 2982-2892.
119. Shirotake, S.; Miyajima, A.; Kosaka, T.; Tanaka, N.; Maeda, T.; Kikuchi, E.; Oya, M. Angiotensin II type 1 receptor expression and microvessel density in human bladder cancer. Urology 2011, 77, e19-e25.
120. Li, D.; Urta, E.; Kimura, T.; Yamamoto, Y.; Osaki, T. Reactive oxygen species (ROS) control the expression of Bcl-2 family proteins by regulating their phosphorylation and ubiquitination. Cancer Sci. 2004, 95, 644-650.
121. Scheit, K.; Bauer, G. Direct and indirect inactivation of tumor cell protective catalase by salicylic acid and anthocyanidins reactivates intercellular ROS signaling and allows for synergistic effects. Carcinogenesis 2015, 36, 400-411.
122. Bauer, G. Central signaling elements of intercellular reactive oxygen/nitrogen species-dependent induction of apoptosis in malignant cells. Anticancer Res. 2017, 37, 499-513.
123. Luanpitpong, S.; Chanvorachote, P.; Stehlik, C.; Tse, W.; Callery, P.S.; Wang, L.; Rojanasakul, Y. Regulation of apoptosis by Bcl-2 cysteine oxidation in human lung epithelial cells. Mol. Biol. Cell 2013, 24, 858-869.
124. Moloney, J.N.; Cotter, T.G. ROS signalling in the biology of cancer. Semin. Cell Dev. Biol. 2017, doi:10.1016/j.semcdb.2017.05.023.
125. Zhao, Y.; Hu, X.; Liu, Y.; Dong, S.; Wen, Z.; He, W.; Zhang, S.; Huang, Q.; Shi, M. ROS signaling under metabolic stress: Cross-talk between AMPK and AKT pathway. Mol. Cancer 2017, 16, 79.
126. Ding, Y.; Ren, K.; Dong, H.; Song, F.; Chen, J.; Guo, Y.; Liu, Y.; Tao, W.; Zhang, Y. Flavonoids from persimmon (Diospyros kaki L.) leaves inhibit proliferation and induce apoptosis in PC-3 cells by activation of oxidative stress and mitochondrial apoptosis. Chem. Biol. Interact. 2017, 275, 210-217.
127. Elkady, A.I. Anethole inhibits the proliferation of human prostate cancer cells via induction of cell cycle arrest and apoptosis. Anticancer Agents Med. Chem. 2017, doi:10.2174/1871520617666170725165717.
128. Deng, Y.; Li, Y.; Yang, F.; Zeng, A.; Yang, S.; Luo, Y.; Zhang, Y.; Xie, Y.; Ye, T.; Xia, Y.; et al. The extract from Punica granatum (pomegranate) peel induces apoptosis and impairs metastasis in prostate cancer cells. Biomed. Pharmacother. 2017, 93, 976-984.
129. Ahmad, M.; Sahabjada; Akhtar, J.; Hussain, A.; Badaruddeen; Arshad, M.; Mishra, A. Development of a new rutin nanoemulsion and its application on prostate carcinoma PC3 cell line. EXCLI J. 2017, 16, 810-823.
130. Lin, J.F.; Tsai, T.F.; Yang, S.C.; Lin, Y.C.; Chen, H.E.; Chou, K.Y.; Hwang, T.I. Benzyl isothiocyanate induces reactive oxygen species-initiated autophagy and apoptosis in human prostate cancer cells. Oncotarget 2017, 8, 20220-20234.
131. Rodriguez-Garcia, A.; Hevia, D.; Mayo, J.C.; Gonzalez-Menendez, P.; Coppo, L.; Lu, J.; Holmgren, A.; Sainz, R.M. Thioredoxin 1 modulates apoptosis induced by bioactive compounds in prostate cancer cells. Redox Biol. 2017, 12, 634-647.
132. Zhu, W.B.; Tian, F.J.; Liu, L.Q. Chikusetsu (CHI) triggers mitochondria-regulated apoptosis in human prostate cancer via reactive oxygen species (ROS) production. Biomed. Pharmacother. 2017, 90, 446-454.
133. Ryu, S.; Lim, W.; Bazer, F.W.; Song, G. Chrysin induces death of prostate cancer cells by inducing ROS and ER stress. J. Cell. Physiol. 2017, 232, 3786-3797.
134. Kim, K.Y.; Kim, S.H.; Yu, S.N.; Park, S.G.; Kim, Y.W.; Nam, H.W.; An, H.H.; Yu, H.S.; Kim, Y.W.; Ji, J.H.; et al. Lasalocid induces cytotoxic apoptosis and cytoprotective autophagy through reactive oxygen species in human prostate cancer PC-3 cells. Biomed. Pharmacother. 2017, 8, 1016-1024.
135. Lim, W.; Park, S.; Bazer, F.W.; Song, G. Naringenin-induced apoptotic cell death in prostate cancer cells Is mediated via the PI3K/AKT and MAPK signaling pathways. J. Cell. Biochem. 2017, 118, 1118-1131.
136. Lim, W.; Jeong, M.; Bazer, F.W.; Song, G. Coumestrol inhibits proliferation and migration of prostate cancer cells by regulating AKT, ERK1/2, and JNK MAPK cell signaling cascades. J. Cell. Physiol. 2017, 232, 862-871.
137. Chen, M.; Zhou, B.; Zhong, P.; Rajamanickam, V.; Dai, X.; Karvannan, K.; Zhou, H.; Zhang, X.; Liang, G. Increased intracellular reactive oxygen species mediates the anti-cancer effects of WZ35 via activating mitochondrial apoptosis pathway in prostate cancer cells. Prostate 2017, 77, 489-504.
138. Kim, K.Y.; Park, K.I.; Kim, S.H.; Yu, S.N.; Park, S.G.; Kim, Y.W.; Seo, Y.K.; Ma, J.Y.; Ahn, S.C. Inhibition of autophagy promotes salinomycin-induced apoptosis via reactive oxygen species-mediated PI3K/AKT/mTOR and ERK/p38 MAPK-dependent signaling in human prostate cancer. Int. J. Mol. Sci. 2017, 18, E1088.
139. Park, S.G.; Kim, S.H.; Kim, K.Y.; Yu, S.N.; Choi, H.D.; Kim, Y.W.; Nam, H.W.; Seo, Y.K.; Ahn, S.C. Toyocamycin induces apoptosis via the crosstalk between reactive oxygen species and p38/ERK MAPKs signaling pathway in human prostate cancer PC-3 cells. Pharmacol. Rep. 2017, 69, 90-96.
140. Qiu, M.; Chen, L.; Tan, G.; Ke, L.; Zhang, S.; Chen, H.; Liu, J. JS-K promotes apoptosis by inducing ROS production in human prostate cancer cells. Oncol. Lett. 2017, 13, 1137-1142.
141. Thamilselvan, V.; Menon, M.; Stein, G.S.; Valeriote, F.; Thamilselvan, S. Combination of carmustine and selenite inhibits EGFR mediated growth signaling in androgen-independent prostate cancer cells. J. Cell. Biochem. 2017, doi:10.1002/jcb.26086.
142. Thamilselvan, V.; Menon, M.; Thamilselvan, S. Combination of carmustine and selenite effectively inhibits tumor growth by targeting androgen receptor, androgen receptor-variants, and Akt in preclinical models: New hope for patients with castration resistant prostate cancer. Int. J. Cancer 2016, 139, 1632-1647.
143. Wright, C.; Iyer, A.K.V.; Kaushik, V.; Azad, N. Anti-tumorigenic potential of a novel orlistat-AICAR combination in prostate cancer cells. J. Cell. Biochem. 2017, doi:10.1002/jcb.26033.
144. Cao, J.; Wang, H.; Chen, F.; Fang, J.; Xu, A.; Xi, W.; Zhang, S.; Wu, G.; Wang, Z. Galangin inhibits cell invasion by suppressing the epithelial-mesenchymal transition and inducing apoptosis in renal cell carcinoma. Mol. Med. Rep. 2016, 13, 4238-4244.
145. Zhong, W.F.; Wang, X.H.; Pan, B.; Li, F.; Kuang, L.; Su, Z.X. Eupatilin induces human renal cancer cell apoptosis via ROS-mediated MAPK and PI3K/AKT signaling pathways. Oncol. Lett. 2016, 12, 2894-2899.
146. Park, J.E.; Park, B.; Chae, I.G.; Kim, D.H.; Kundu, J.; Kundu, J.K.; Chun, K.S. Carnosic acid induces apoptosis through inactivation of Src/STAT3 signaling pathway in human renal carcinoma Caki cells. Oncol. Rep. 2016, 35, 2723-2732.
147. Wu, J.; Zheng, W.; Rong, L.; Xing, Y.; Hu, D. Bicyclol exerts an anti-tumor effect via ROS-mediated endoplasmic reticulum stress in human renal cell carcinoma cells. Biomed. Pharmacother. 2017, 91, 1184-1192.
148. Zhao, J.; He, Q.; Gong, Z.; Chen, S.; Cui, L. Niclosamide suppresses renal cell carcinoma by inhibiting Wnt/β-catenin and inducing mitochondrial dysfunctions. Springerplus 2016, 5, 1436.
149. Yin, P.; Jia, J.; Li, J.; Song, Y.; Zhang, Y.; Chen, F. ABT-737, a Bcl-2 selective inhibitor, and chloroquine synergistically kill renal cancer cells. Oncol. Res. 2016, 24, 65-72.
150. Gillissen, B.; Richter, A.; Richter, A.; Preissner, R.; Schulze-Osthoff, K.; Essmann, F.; Daniel, P.T. Bax/Bakindependent mitochondrial depolarization and reactive oxygen species induction by sorafenib overcome resistance to apoptosis in renal cell carcinoma. J. Biol. Chem. 2017, 292, 6478-6492.
151. Wang, L.; Azad, N.; Kongkaneramit, L.; Chen, F.; Lu, Y.; Jiang, B.H.; Rojanasakul, Y. The Fas death signaling pathway connecting reactive oxygen species generation and FLICE inhibitory protein down-regulation. J. Immunol. 2008, 180, 3072-3080.
152. Lee, S.J.; Noh, H.J.; Sung, E.G.; Song, I.H.; Kim, J.Y.; Kwon, T.K.; Lee, T.J. Berberine sensitizes TRAILinduced apoptosis through proteasome-mediated downregulation of c-FLIP and Mcl-1 proteins. Int. J. Oncol. 2011, 38, 485-492.
153. Han, M.A.; Woo, S.M.; Min, K.J.; Kim, S.; Park, J.W.; Kim, D.E.; Kim, S.H.; Choi, Y.H.; Kwon, T.K. 6-Shogaol enhances renal carcinoma Caki cells to TRAIL-induced apoptosis through reactive oxygen speciesmediated cytochrome c release and down-regulation of c-FLIP(L) expression. Chem. Biol. Interact. 2015, 228, 69-78.
154. Park, E.J.; Chauhan, A.K.; Min, K.J.; Park, D.C.; Kwon, T.K. Thymoquinone induces apoptosis through downregulation of c-FLIP and Bcl-2 in renal carcinoma Caki cells. Oncol. Rep. 2016, 36, 2261-2267.
155. Lu, C.C.; Shen, C.H.; Chang, C.B.; Hsieh, H.Y.; Wu, J.D.; Tseng, L.H.; Hwang, D.W.; Chen, S.Y.; Wu, S.F.; Chan, M.W.; et al. Guizhi Fuling Wan as a novel agent for intravesical treatment for bladder cancer in mouse model. Mol. Med. 2017, doi:10.2119/molmed.2015.00085.
156. Romanov, V.; Whyard, T.C.; Waltzer, W.C.; Grollman, A.P.; Rosenquist, T. Aristolochic acid-induced apoptosis and G2 cell cycle arrest depends on ROS generation and MAP kinases activation. Arch. Toxicol. 2015, 89, 47-56.
157. Li, Y.; Wen, J.M.; Du, C.J.; Hu, S.M.; Chen, J.X.; Zhang, S.G.; Zhang, N.; Gao, F.; Li, S.J.; Mao, X.W.; et al. Thymol inhibits bladder cancer cell proliferation via inducing cell cycle arrest and apoptosis. Biochem. Biophys. Res. Commun. 2017, doi:10.1016/j.bbrc.2017.04.009.
158. Qiu, M.; Chen, L.; Tan, G.; Ke, L.; Zhang, S.; Chen, H.; Liu, J. A reactive oxygen species activation mechanism contributes to JS-K-induced apoptosis in human bladder cancer cells. Sci. Rep. 2015, 5, 15104
159. Yu, G.Q.; Dou, Z.L.; Jia, Z.H. 5-bromo-3-(3-hydroxyprop-1-ynyl)-2H-pyran-2-one induces apoptosis in T24 human bladder cancer cells through mitochondria-dependent signaling pathways. Mol. Med. Rep. 2017, 15, 153-159.
160. Saleem, A.; Dvorzhinski, D.; Santanam, U.; Mathew, R.; Bray, K.; Stein, M.; White, E.; DiPaola, R.S. Effect of dual inhibition of apoptosis and autophagy in prostate cancer. Prostate 2012, 72, 1374-1381.
161. Hsin, I.L.; Wang, S.C.; Li, J.R.; Ciou, T.C.; Wu, C.H.; Wu, H.M.; Ko, J.L. Immunomodulatory proteins FIPgts and chloroquine induce caspase-independent cell death via autophagy for resensitizing cisplatinresistant urothelial cancer cells. Phytomedicine 2016, 23, 1566-1573.