ROS signalling in the biology of cancer

Seminars in Cell and Developmental Biology

Volumn 80, Issue , 2018, Pages 50-64

  Moloney, Jennifer N ^a   Cotter, Thomas G ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Antioxidants; Cancer; Reactive oxygen species (ROS); Signalling; Therapy

Indexed keywords

CYTOCHROME P450; DNA; LIPOXYGENASE; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE; ANTIOXIDANT;

ADAPTATION; AUTOPHAGY; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; DNA DAMAGE; DRUG RESISTANCE; GENOMIC INSTABILITY; HUMAN; MALIGNANT NEOPLASM; MITOCHONDRION; OXIDATIVE STRESS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TUMOR CELL; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; NEOPLASM; PHYSIOLOGY;

ANIMALS; ANTIOXIDANTS; DNA DAMAGE; HUMANS; NEOPLASMS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 85020436220     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2017.05.023     Document Type: Review

References (276)

1. Giorgio, M., Trinei, M., Migliaccio, E., Pelicci, P.G., Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals?. Nat. Rev. Mol. Cell Biol. 8:9 (2007), 722–728.
2. Zorov, D.B., Juhaszova, M., Sollott, S.J., Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94:3 (2014), 909–950.
3. Panieri, E., Santoro, M.M., ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell. Death Dis., 7, 2016, e2253.
4. Liou, G.-Y., Storz, P., Reactive oxygen species in cancer. Free Radic. Res. 44:5 (2010), 479–496.
5. Roy, K., Wu, Y., Meitzler, Jennifer L., Juhasz, A., Liu, H., Jiang, G., Lu, J., Antony, S., Doroshow, James H., NADPH oxidases and cancer. Clin. Sci. 128:12 (2015), 863–875.
6. Stanicka, J., Russell, E.G., Woolley, J.F., Cotter, T.G., NADPH oxidase-generated hydrogen peroxide induces DNA damage in mutant FLT3-expressing leukemia cells. J. Biol. Chem. 290:15 (2015), 9348–9361.
7. Ames, B.N., Shigenaga, M.K., Hagen, T.M., Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U. S. A. 90:17 (1993), 7915–7922.
8. Szatrowski, T.P., Nathan, C.F., Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51:3 (1991), 794–798.
9. Sabharwal, S.S., Schumacker, P.T., Mitochondrial ROS in cancer: initiators, amplifiers or an Achilles’ heel?. Nat. Rev. Cancer 14:11 (2014), 709–721.
10. Moloney, J.N., Stanicka, J., Cotter, T.G., Subcellular localization of the FLT3-ITD oncogene plays a significant role in the production of NOX- and p22phox-derived reactive oxygen species in acute myeloid leukemia. Leuk. Res. 52 (2017), 34–42.
11. Vander Heiden, M.G., Cantley, L.C., Thompson, C.B., Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science (New York N.Y.) 324:5930 (2009), 1029–1033.
12. Levine, A.J., Puzio-Kuter, A.M., The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330:6009 (2010), 1340–1344.
13. Gorrini, C., Harris, I.S., Mak, T.W., Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12:12 (2013), 931–947.
14. Pelicano, H., Carney, D., Huang, P., ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 7:2 (2004), 97–110.
15. Nogueira, V., Park, Y., Chen, C.-C., Xu, P.-Z., Chen, M.-L., Tonic, I., Unterman, T., Hay, N., Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 14:6 (2008), 458–470.
16. Trachootham, D., Zhou, Y., Zhang, H., Demizu, Y., Chen, Z., Pelicano, H., Chiao, P.J., Achanta, G., Arlinghaus, R.B., Liu, J., Huang, P., Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell 10:3 (2006), 241–252.
17. Storz, P., Reactive oxygen species in tumor progression. Front. Biosci. 10:1–3 (2005), 1881–1896.
18. Dickinson, B.C., Chang, C.J., Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 7:8 (2011), 504–511.
19. Jayavelu, A.K., Moloney, J.N., Böhmer, F.-D., Cotter, T.G., NOX-driven ROS formation in cell transformation of FLT3-ITD-positive AML. Exp. Hematol. 44:12 (2016), 1113–1122.
20. Winterbourn, C.C., Hampton, M.B., Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45:5 (2008), 549–561.
21. Finkel, T., Signal transduction by reactive oxygen species. J. Cell Biol. 194:1 (2011), 7–15.
22. Reczek, C.R., Chandel, N.S., ROS-dependent signal transduction. Curr. Opin. Cell Biol. 33 (2015), 8–13.
23. Davies, M.J., The oxidative environment and protein damage. Biochim. Biophys. Acta (BBA)—Proteins Proteom. 1703:2 (2005), 93–109.
24. Miki, H., Funato, Y., Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species. J. Biochem. 151:3 (2012), 255–261.
25. Hawkes, W.C., Alkan, Z., Regulation of redox signaling by selenoproteins. Biol. Trace Elem. Res. 134:3 (2010), 235–251.
26. Hoshi, T., Heinemann, S.H., Regulation of cell function by methionine oxidation and reduction. J. Physiol. 531:Pt 1 (2001), 1–11.
27. Lee, J.-W., Helmann, J.D., The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440:7082 (2006), 363–367.
28. Groeger, G., Quiney, C., Cotter, T.G., Hydrogen peroxide as a cell-survival signaling molecule. Antioxid. Redox Signal. 11:11 (2009), 2655–2671.
29. Veal, E.A., Day, A.M., Morgan, B.A., Hydrogen peroxide sensing and signaling. Mol. Cell 26:1 (2007), 1–14.
30. Jayavelu, A.K., Muller, J.P., Bauer, R., Bohmer, S.A., Lassig, J., Cerny-Reiterer, S., Sperr, W.R., Valent, P., Maurer, B., Moriggl, R., Schroder, K., Shah, A.M., Fischer, M., Scholl, S., Barth, J., Oellerich, T., Berg, T., Serve, H., Frey, S., Fischer, T., Heidel, F.H., Bohmer, F.D., NOX4-driven ROS formation mediates PTP inactivation and cell transformation in FLT3ITD-positive AML cells. Leukemia 30:2 (2016), 473–483.
31. Holmstrom, K.M., Finkel, T., Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 15:6 (2014), 411–421.
32. 2 for platelet-derived growth factor signal transduction. Science 270:5234 (1995), 296–299.
33. Kröller-Schön, S., Steven, S., Kossmann, S., Scholz, A., Daub, S., Oelze, M., Xia, N., Hausding, M., Mikhed, Y., Zinßius, E., Mader, M., Stamm, P., Treiber, N., Scharffetter-Kochanek, K., Li, H., Schulz, E., Wenzel, P., Münzel, T., Daiber, A., 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. 20:2 (2014), 247–266.
34. Handy, D.E., Loscalzo, J., Redox regulation of mitochondrial function. Antioxid. Redox Signal. 16:11 (2012), 1323–1367.
35. Quinlan, C.L., Treberg, J.R., Perevoshchikova, I.V., Orr, A.L., Brand, M.D., Native rates of superoxide production from multiple sites in isolated mitochondria measured using endogenous reporters. Free Rad. Biol. Med. 53:9 (2012), 1807–1817.
36. Goncalves, R.L.S., Quinlan, C.L., Perevoshchikova, I.V., Hey-Mogensen, M., Brand, M.D., Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise. J. Biol. Chem. 290:1 (2015), 209–227.
37. Murphy, Michael P., How mitochondria produce reactive oxygen species. Biochem. J. 417:Pt 1 (2009), 1–13.
38. Muller, F.L., Liu, Y., Van Remmen, H., Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 279:47 (2004), 49064–49073.
39. Sena, L.A., Chandel, N.S., Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 48:2 (2012), 158–167.
40. Han, D., Williams, E., Cadenas, E., Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem. J. 353:Pt 2 (2001), 411–416.
41. Bienert, G.P., Møller, A.L.B., Kristiansen, K.A., Schulz, A., Møller, I.M., Schjoerring, J.K., Jahn, T.P., Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282:2 (2007), 1183–1192.
42. Jitschin, R., Hofmann, A.D., Bruns, H., Gießl, A., Bricks, J., Berger, J., Saul, D., Eckart, M.J., Mackensen, A., Mougiakakos, D., Mitochondrial metabolism contributes to oxidative stress and reveals therapeutic targets in chronic lymphocytic leukemia. Blood 123:17 (2014), 2663–2672.
43. Hart, P.C., Mao, M., de Abreu, A.L.P., Ansenberger-Fricano, K., Ekoue, D.N., Ganini, D., Kajdacsy-Balla, A., Diamond, A.M., Minshall, R.D., Consolaro, M.E.L., Santos, J.H., Bonini, M.G., MnSOD upregulation sustains the Warburg effect via mitochondrial ROS and AMPK-dependent signalling in cancer. Nat. Commun., 6, 2015, 6053.
44. Bedard, K., Krause, K.-H., The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:1 (2007), 245–313.
45. Brewer, T.F., Garcia, F.J., Onak, C.S., Carroll, K.S., Chang, C.J., Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NADPH oxidase proteins. Annu. Rev. Biochem. 84:1 (2015), 765–790.
46. Bienert, G.P., Chaumont, F., Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim. Biophys. Acta (BBA)—Gen. Subj. 1840:5 (2014), 1596–1604.
47. Jackson, S.H., Devadas, S., Kwon, J., Pinto, L.A., Williams, M.S., T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 5:8 (2004), 818–827.
48. Richards, S.M., Clark, E.A., BCR-induced superoxide negatively regulates B cell proliferation and t cell-independent type 2 antibody responses. Eur. J. Immunol. 39:12 (2009), 3395–3403.
49. Naughton, R., Quiney, C., Turner, S.D., Cotter, T.G., Bcr-Abl-mediated redox regulation of the PI3 K/AKT pathway. Leukemia 23:8 (2009), 1432–1440.
50. Woolley, J.F., Naughton, R., Stanicka, J., Gough, D.R., Bhatt, L., Dickinson, B.C., Chang, C.J., Cotter, T.G., H2O2 production downstream of FLT3 is mediated by p22phox in the endoplasmic reticulum and is required for STAT5 signalling. PLoS One, 7(7), 2012, e34050.
51. Brown, D.I., Griendling, K.K., Nox proteins in signal transduction. Free Radic. Biol. Med. 47:9 (2009), 1239–1253.
52. Brandes, R.P., Weissmann, N., Schröder, K., Nox family NADPH oxidases: molecular mechanisms of activation. Free Radic. Biol. Med. 76 (2014), 208–226.
53. Ambasta, R.K., Kumar, P., Griendling, K.K., Schmidt, H.H.H.W., Busse, R., Brandes, R.P., Direct interaction of the novel nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279:44 (2004), 45935–45941.
54. Groemping, Y., Rittinger, K., Activation and assembly of the NADPH oxidase: a structural perspective. Biochem. J 386:Pt 3 (2005), 401–416.
55. Groemping, Y., Lapouge, K., Smerdon, S.J., Rittinger, K., Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113:3 (2003), 343–355.
56. Sumimoto, H., Hata, K., Mizuki, K., Ito, T., Kage, Y., Sakaki, Y., Fukumaki, Y., Nakamura, M., Takeshige, K., Assembly and activation of the phagocyte NADPH oxidase: specific interaction of the N-terminal src homology 3 domain of p47phox WITH p22phox IS required for activation of the nadph oxidase. J. Biol. Chem. 271:36 (1996), 22152–22158.
57. Ago, T., Kitazono, T., Kuroda, J., Kumai, Y., Kamouchi, M., Ooboshi, H., Wakisaka, M., Kawahara, T., Rokutan, K., Ibayashi, S., Iida, M., NAD(P)H oxidases in rat basilar arterial endothelial cells. Stroke 36:5 (2005), 1040–1046.
58. Kobayashi, S., Nojima, Y., Shibuya, M., Maru, Y., Nox1 regulates apoptosis and potentially stimulates branching morphogenesis in sinusoidal endothelial cells. Exp. Cell Res. 300:2 (2004), 455–462.
59. + channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 287:5450 (2000), 138–142.
60. Cheng, G., Diebold, B.A., Hughes, Y., Lambeth, J.D., Nox1-dependent reactive oxygen generation is regulated by Rac1. J. Biol. Chem. 281:26 (2006), 17718–17726.
61. Bánfi, B., Malgrange, B., Knisz, J., Steger, K., Dubois-Dauphin, M., Krause, K.-H., NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279:44 (2004), 46065–46072.
62. Ueno, N., Takeya, R., Miyano, K., Kikuchi, H., Sumimoto, H., The NADPH oxidase nox3 constitutively produces superoxide in a p22phox-dependent manner: its regulation by oxidase organizers and activators. J. Biol. Chem. 280:24 (2005), 23328–23339.
63. Cheng, G., Cao, Z., Xu, X., Meir, E.G.V., Lambeth, J.D., Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269:1–2 (2001), 131–140.
64. 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 133:5 (2007), 1637–1648.
65. Maloney, E., Sweet, I.R., Hockenbery, D.M., Pham, 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 29:9 (2009), 1370–1375.
66. Liu, R.-M., Choi, J., Wu, J.-H., Gaston Pravia, K.A., Lewis, K.M., Brand, J.D., Mochel, N.S.R., Krzywanski, D.M., Lambeth, J.D., Hagood, J.S., Forman, H.J., Thannickal, V.J., Postlethwait, E.M., Oxidative modification of nuclear mitogen-activated protein kinase phosphatase 1 is involved in transforming growth factor β1-induced expression of plasminogen activator inhibitor 1 in fibroblasts. J. Biol. Chem. 285:21 (2010), 16239–16247.
67. Mandal, Chandi C., Ganapathy, S., Gorin, Y., Mahadev, K., Block, K., Abboud, Hanna E., Harris, Stephen E., Ghosh-Choudhury, G., Ghosh-Choudhury, N., Reactive oxygen species derived from Nox4 mediate BMP2 gene transcription and osteoblast differentiation. Biochem. J. 433:2 (2011), 393–402.
68. Edderkaoui, M., Nitsche, C., Zheng, L., Pandol, S.J., Gukovsky, I., Gukovskaya, A.S., NADPH oxidase activation in pancreatic cancer cells is mediated through akt-dependent up-regulation of p22phox. J. Biol. Chem. 286:10 (2011), 7779–7787.
69. Donkó Á., Péterfi, Z., Sum, Á., Leto, T., Geiszt, M., Dual oxidases. Phil. Trans. R. Soc. B: Biol. Sci. 360:1464 (2005), 2301–2308.
70. Bánfi, B., Tirone, F., Durussel, I., Knisz, J., Moskwa, P., Molnár, G.Z., Krause, K.-H., Cox, J.A., Mechanism of Ca2+ activation of the NADPH oxidase 5 (NOX5). J. Biol. Chem. 279:18 (2004), 18583–18591.
71. Kawahara, T., Ritsick, D., Cheng, G., Lambeth, J.D., Point mutations in the proline-rich region of p22phox are dominant inhibitors of nox1- and nox2-dependent reactive oxygen generation. J. Biol. Chem. 280:36 (2005), 31859–31869.
72. Bedard, K., Jaquet, V., Krause, K.-H., NOX5: from basic biology to signaling and disease. Free Radic. Biol. Med. 52:4 (2012), 725–734.
73. Shah, A.M., Parsing the role of nox enzymes and ros in heart failure. Circulation, 2015.
74. Usui, S., Oveson, B.C., Lee, S.Y., Jo, Y.-J., Yoshida, T., Miki, A., Miki, K., Iwase, T., Lu, L., Campochiaro, P.A., NADPH oxidase plays a central role in cone cell death in retinitis pigmentosa. J. Neurochem. 110:3 (2009), 1028–1037.
75. Gorin, Y., Block, K., Nox as a target for diabetic complications. Clin. Sci. 125:8 (2013), 361–382.
76. van der Vliet, A., Nox enzymes in allergic airway inflammation. Biochim. Biophys. Acta 1810:11 (2011), 1035–1044.
77. Gao, H.-M., Zhou, H., Hong, J.-S., NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol. Sci. 33:6 (2012), 295–303.
78. Gough, D.R., Cotter, T.G., Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis., 2, 2011, e213.
79. Block, K., Gorin, Y., Aiding and abetting roles of NOX oxidases in cellular transformation. Nat. Rev. Cancer 12:9 (2012), 627–637.
80. Shimada, K., Nakamura, M., Anai, S., A novel human AlkB homologue, ALKBH8, contributes to human bladder cancer progression. Cancer Res. 69:7 (2009), 3157–3164.
81. Shimada, K., Fujii, T., Anai, S., Fujimoto, K., Konishi, N., ROS generation via NOX4 and its utility in the cytological diagnosis of urothelial carcinoma of the urinary bladder. BMC Urol., 11, 2011 22-22.
82. Graham, K.A., Kulawiec, M., Owens, K.M., Li, X., Desouki, M.M., Chandra, D., Singh, K.K., NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol. Ther. 10:3 (2010), 223–231.
83. Desouki, M.M., Kulawiec, M., Bansal, S., Das, G.C., Singh, K.K., Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biol. Ther. 4:12 (2005), 1367–1373.
84. Choi, J.-A., Lee, J.-W., Kim, H., Kim, E.-Y., Seo, J.-M., Ko, J., Kim, J.-H., Pro-survival of estrogen receptor-negative breast cancer cells is regulated by a BLT2?reactive oxygen species-linked signaling pathway. Carcinogenesis 31:4 (2010), 543–551.
85. Juhasz, A., Ge, Y.U.N., Markel, S., Chiu, A., Matsumoto, L., Van Balgooy, 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. 43:6 (2009), 523–532.
86. Fukuyama, M., Rokutan, K., Sano, T., Miyake, H., Shimada, M., Tashiro, S., Overexpression of a novel superoxide-producing enzyme, NADPH oxidase 1, in adenoma and well differentiated adenocarcinoma of the human colon. Cancer Lett. 221:1 (2005), 97–104.
87. Bauer, K.M., Hummon, A.B., Buechler, S., Right-side and left-side colon cancer follow different pathways to relapse. Mol. Carcinog. 51:5 (2012), 411–421.
88. Block, K., Gorin, Y., New, D.D., Eid, A., Chelmicki, T., Reed, A., Choudhury, G.G., Parekh, D.J., Abboud, H.E., The NADPH oxidase subunit p22phox inhibits the function of the tumor suppressor protein tuberin. Am. J. Pathol. 176:5 (2010), 2447–2455.
89. 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. 282:11 (2007), 8019–8026.
90. Prata, C., Maraldi, T., Fiorentini, D., Zambonin, L., Hakim, G., Landi, L., Nox-generated ROS modulate glucose uptake in a leukaemic cell line. Free Radic. Res. 42:5 (2008), 405–414.
91. Kamiguti, A.S., Serrander, L., Lin, K., Harris, R.J., Cawley, J.C., Allsup, D.J., Slupsky, J.R., Krause, K.-H., Zuzel, M., Expression and activity of NOX5 in the circulating malignant B cells of hairy cell leukemia. J. Immunol. 175:12 (2005), 8424–8430.
92. Han, M., Zhang, T., Yang, L., Wang, Z., Ruan, J., Chang, X., Association between NADPH oxidase (NOX) and lung cancer: a systematic review and meta-analysis. J. Thorac. Dis. 8:7 (2016), 1704–1711.
93. Luxen, S., Belinsky, S.A., Knaus, U.G., Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res. 68:4 (2008), 1037–1045.
94. Brar, S.S., Kennedy, T.P., Sturrock, A.B., Huecksteadt, T.P., Quinn, M.T., Whorton, A.R., Hoidal, J.R., An NAD(P)H oxidase regulates growth and transcription in melanoma cells. Am. J. Physiol.—Cell Physiol. 282:6 (2002), C1212–C1224.
95. Fu, X., Beer, D.G., Behar, J., Wands, J., Lambeth, D., Cao, W., CAMP-response element-binding protein mediates acid-induced NADPH oxidase NOX5-S expression in barrett esophageal adenocarcinoma cells. J. Biol. Chem. 281:29 (2006), 20368–20382.
96. 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. 67:22 (2007), 10823–10830.
97. Vaquero, E.C., Edderkaoui, M., Pandol, S.J., Gukovsky, I., Gukovskaya, A.S., Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J. Biol. Chem. 279:33 (2004), 34643–34654.
98. 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. Pathol. 171:6 (2007), 2021–2032.
99. Lim, S.D., Sun, C., Lambeth, J.D., Marshall, F., Amin, M., Chung, L., Petros, J.A., Arnold, R.S., Increased Nox1 and hydrogen peroxide in prostate cancer. Prostate 62:2 (2005), 200–207.
100. Kumar, B., Koul, S., Khandrika, L., Meacham, R.B., Koul, H.K., Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 68:6 (2008), 1777–1785.
101. Brar, S.S., Corbin, Z., Kennedy, T.P., Hemendinger, R., Thornton, L., Bommarius, B., Arnold, R.S., Whorton, A.R., Sturrock, A.B., Huecksteadt, T.P., Quinn, M.T., Krenitsky, K., Ardie, K.G., Lambeth, J.D., Hoidal, J.R., NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am. J. Physiol.—Cell Physiol. 285:2 (2003), C353–C369.
102. Huang, W.-C., Li, X., Liu, J., Lin, J., Chung, L.W.K., 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. 10:1 (2012), 133–142.
103. Pettigrew, C.A., Clerkin, J.S., Cotter, T.G., DUOX enzyme activity promotes AKT signalling in prostate cancer cells. Anticancer Res. 32:12 (2012), 5175–5181.
104. Kawahara, T., Kohjima, M., Kuwano, Y., Mino, H., Teshima-Kondo, S., Takeya, R., Tsunawaki, S., Wada, A., Sumimoto, H., Rokutan, K., Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase Nox1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am. J. Physiol.—Cell Physiol. 288:2 (2005), C450–C457.
105. Weyemi, U., Caillou, B., Talbot, M., Ameziane-El-Hassani, R., Lacroix, L., Lagent-Chevallier, O., Al Ghuzlan, A., Roos, D., Bidart, J.-M., Virion, A., Schlumberger, M., Dupuy, C., Intracellular expression of reactive oxygen species-generating NADPH oxidase NOX4 in normal and cancer thyroid tissues. Endocr. Relat. Cancer 17:1 (2010), 27–37.
106. Bertagnolli, M.M., The potential of non-steroidal anti-inflammatory drugs (NSAIDs) for colorectal cancer prevention. J. Surg. Oncol. 84:3 (2003), 113–119.
107. Collet, J.P., Sharpe, C., Belzile, E., Boivin, J.F., Hanley, J., Abenhaim, L., Colorectal cancer prevention by non-steroidal anti-inflammatory drugs: effects of dosage and timing. Br. J. Cancer 81:1 (1999), 62–68.
108. Huls, G., Koornstra, J.J., Kleibeuker, J.H., Non-steroidal anti-inflammatory drugs and molecular carcinogenesis of colorectal carcinomas. Lancet 362:9379 (2003), 230–232.
109. Marnett, L.J., DuBois, R.N., COX-2: A target for colon cancer prevention. Ann. Rev. Pharmacol. Toxicol., 2002, 55–80.
110. Moran, E.M., Epidemiological and clinical aspects of nonsteroidal anti-inflammatory drugs and cancer risks. J. Environ. Pathol. Toxicol. Oncol. 21:2 (2002), 193–201.
111. Thun, M.J., Henley, S.J., Patrono, C., Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J. Natl. Cancer Inst. 94:4 (2002), 252–266.
112. Fukai, T., Ushio-Fukai, M., Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid. Redox Signal. 15:6 (2011), 1583–1606.
113. Bendayan, M., Reddy, J.K., Immunocytochemical localization of catalase and heat-labile enoyl-CoA hydratase in the livers of normal and peroxisome proliferator-treated rats. Lab. Invest. 47:4 (1982), 364–369.
114. 2. J. Biochem. 108:3 (1990), 426–431.
115. Litwin, J.A., Völkl, A., Müller-Höcker, J., Hashimoto, T., Fahimi, H.D., Immunocytochemical localization of peroxisomal enzymes in human liver biopsies. Am. J. Pathol. 128:1 (1987), 141–150.
116. Wood, Z.A., Schröder, E., Robin Harris, J., Poole, L.B., Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:1 (2003), 32–40.
117. Cox, Andrew G., Winterbourn, Christine C., Hampton, Mark B., Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J 425:2 (2010), 313–325.
118. Arteel, G.E., Sies, H., The biochemistry of selenium and the glutathione system. Environ. Toxicol. Pharmacol. 10:4 (2001), 153–158.
119. Janssen, A.M.L., Bosman, C.B., Kruidenier, L., Griffioen, G., Lamers, C.B.H.W., van Krieken, J.H.J.M., van de Velde, C.J.H., Verspaget, H.W., Superoxide dismutases in the human colorectal cancer sequence. J. Cancer Res. Clin. Oncol. 125:6 (1999), 327–335.
120. Miranda, A., Janssen, L., Bosman, C.B., van Duijn, W., Oostendorp-van de Ruit, M.M., Kubben, F.J.G.M., Griffioen, G., Lamers, C.B.H.W., Han, J., van Krieken, J.M., van de Velde, C.J.H., Verspaget, H.W., Superoxide dismutases in gastric and esophageal cancer and the prognostic impact in gastric cancer. Clin. Cancer Res. 6:8 (2000), 3183–3192.
121. Toledano, M.B., Planson, A.-G., Delaunay-Moisan, A., Reining in H2O2 for safe signaling. Cell 140:4 (2010), 454–456.
122. Leslie, N.R., Bennett, D., Lindsay, Y.E., Stewart, H., Gray, A., Downes, C., Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 22:20 (2003), 5501–5510.
123. Harris, I.S., Blaser, H., Moreno, J., Treloar, A.E., Gorrini, C., Sasaki, M., Mason, J.M., Knobbe, C.B., Rufini, A., Halle, M., Elia, A.J., Wakeham, A., Tremblay, M.L., Melino, G., Done, S., Mak, T.W., PTPN12 promotes resistance to oxidative stress and supports tumorigenesis by regulating FOXO signaling. Oncogene 33:8 (2014), 1047–1054.
124. Lee, S.-R., Yang, K.-S., Kwon, J., Lee, C., Jeong, W., Rhee, S.G., Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 277:23 (2002), 20336–20342.
125. Sarsour, E.H., Venkataraman, S., Kalen, A.L., Oberley, L.W., Goswami, P.C., Manganese superoxide dismutase activity regulates transitions between quiescent and proliferative growth. Aging cell 7:3 (2008), 405–417.
126. Wang, M., Kirk, J.S., Venkataraman, S., Domann, F.E., Zhang, H.J., Schafer, F.Q., Flanagan, S.W., Weydert, C.J., Spitz, D.R., Buettner, G.R., Oberley, L.W., Manganese superoxide dismutase suppresses hypoxic induction of hypoxia-inducible factor-1[alpha] and vascular endothelial growth factor. Oncogene 24:55 (2005), 8154–8166.
127. Khavari, T.A., Rinn, J.L., Ras/Erk MAPK signaling in epidermal homeostasis and neoplasia. ABBV Cell Cycle 6:23 (2007), 2928–2931.
128. Roberts, P.J., Der, C.J., Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 26:22 (2007), 3291–3310.
129. Irani, K., Xia, Y., Zweier, J.L., Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275:5306 (1997), 1649–1652.
130. Reddy, K.B., Glaros, S., Inhibition of the MAP kinase activity suppresses estrogen-induced breast tumor growth both in vitro and in vivo. Int. J. Oncol. 30:4 (2007), 971–976.
131. Burdick, A.D., Davis, J.W., Liu, K.J., Hudson, L.G., Shi, H., Monske, M.L., Burchiel, S.W., Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in Breast epithelial cells. Cancer Res. 63:22 (2003), 7825–7833.
132. Park, S.-A., Na, H.-K., Kim, E.-H., Cha, Y.-N., Surh, Y.-J., 4-Hydroxyestradiol induces anchorage-independent growth of human mammary epithelial cells via activation of IκB kinase: potential role of reactive oxygen species. Cancer Res. 69:6 (2009), 2416–2424.
133. McCubrey, J.A., Steelman, L.S., Chappell, W.H., Abrams, S.L., Wong, E.W.T., Chang, F., Lehmann, B., Terrian, D.M., Milella, M., Tafuri, A., Stivala, F., Libra, M., Basecke, J., Evangelisti, C., Martelli, A.M., Franklin, R.A., Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim. Biophys. Acta 1773:8 (2007), 1263–1284.
134. Steelman, L.S., Abrams, S.L., Whelan, J., Bertrand, F.E., Ludwig, D.E., Basecke, J., Libra, M., Stivala, F., Milella, M., Tafuri, A., Lunghi, P., Bonati, A., Martelli, A.M., McCubrey, J.A., Contributions of the Raf//MEK//ERK, PI3 K//PTEN//Akt//mTOR and Jak//STAT pathways to leukemia. Leukemia 22:4 (2008), 686–707.
135. Chan, D.W., Liu, V.W.S., Tsao, G.S.W., Yao, K.-M., Furukawa, T., Chan, K.K.L., Ngan, H.Y.S., Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 29:9 (2008), 1742–1750.
136. Lee, W.C., Choi, C.H., Cha, S.H., Oh, H.L., Kim, Y.K., Role of ERK in hydrogen peroxide-Induced cell death of human glioma cells. Neurochem. Res. 30:2 (2005), 263–270.
137. Rygiel, T.P., Mertens, A.E., Strumane, K., van der Kammen, R., Collard, J.G., The Rac activator Tiam1 prevents keratinocyte apoptosis by controlling ROS-mediated ERK phosphorylation. J. Cell Sci. 121:8 (2008), 1183–1192.
138. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J., Greenberg, M.E., Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96:6 (1999), 857–868.
139. Kawamura, N., Kugimiya, F., Oshima, Y., Ohba, S., Ikeda, T., Saito, T., Shinoda, Y., Kawasaki, Y., Ogata, N., Hoshi, K., Akiyama, T., Chen, W.S., Hay, N., Tobe, K., Kadowaki, T., Azuma, Y., Tanaka, S., Nakamura, K., Chung, U.-i., Kawaguchi, H., Akt1 in osteoblasts and osteoclasts controls bone remodeling. PLoS One, 2(10), 2007, e1058.
140. Limaye, V., Li, C., Xia, P., Berndt, M.C., Vadas, M.A., Gamble, J.R., Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1?dependent activation of PI-3 K/Akt and regulation of Bcl-2 family members. Blood 105:8 (2005), 3169–3177.
141. Pastorino, J.G., Tafani, M., Farber, J.L., Tumor necrosis factor induces phosphorylation and translocation of BAD through a phosphatidylinositide-3-OH kinase-dependent pathway. J. Biol. Chem. 274:27 (1999), 19411–19416.
142. Qi, X.-J., Wildey, G.M., Howe, P.H., Evidence that ser87 of BimEL is phosphorylated by akt and regulates BimEL apoptotic function. J. Biol. Chem. 281:2 (2006), 813–823.
143. Xin, M., Deng, X., Nicotine inactivation of the proapoptotic function of bax through phosphorylation. J. Biol. Chem. 280:11 (2005), 10781–10789.
144. Liu, L.-Z., Hu, X.-W., Xia, C., He, J., Zhou, Q., Shi, X., Fang, J., Jiang, B.-H., Reactive oxygen species regulate epidermal growth factor-induced vascular endothelial growth factor and hypoxia-inducible factor-1α expression through activation of AKT and P70S6K1 in human ovarian cancer cells. Free Radic. Biol. Med. 41:10 (2006), 1521–1533.
145. Salmeen, A., Andersen, J.N., Myers, M.P., Meng, T.-C., Hinks, J.A., Tonks, N.K., Barford, D., Redox regulation of protein tyrosine phosphatase 1 B involves a sulphenyl-amide intermediate. Nature 423:6941 (2003), 769–773.
146. Wu, H., Goel, V., Haluska, F.G., PTEN signaling pathways in melanoma. Oncogene 22:20 (2003), 3113–3122.
147. Döppler, H., Storz, P., Mitochondrial and oxidative stress-Mediated activation of protein kinase D1 and its importance in pancreatic cancer. Front. Oncol., 7, 2017, 41.
148. Rozengurt, E., Rey, O., Waldron, R.T., Protein kinase d signaling. J. Biol. Chem. 280:14 (2005), 13205–13208.
149. Wei, N., Chu, E., Wipf, P., Schmitz, J.C., Protein kinase d as a potential chemotherapeutic target for colorectal cancer. Mol. Cancer Ther. 13:5 (2014), 1130–1141.
150. Eiseler, T., Döppler, H., Yan, I.K., Goodison, S., Storz, P., Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion. Breast Cancer Res.: BCR, 11(1), 2009 R13-R13.
151. Song, J., Li, J., Lulla, A., Evers, B.M., Chung, D.H., Protein kinase D protects against oxidative stress-Induced intestinal epithelial cell injury via Rho/ROK/PKC-δ pathway activation, american journal of physiology. Cell Physiol. 290:6 (2006), C1469–C1476.
152. Storz, P., Toker, A., Protein kinase D mediates a stress-induced NF-(B activation and survival pathway. EMBO J. 22:1 (2003), 109–120.
153. Storz, P., Toker, A., NF-κB signaling an alternate pathway for oxidate stress responses. ABBV Cell Cycle 2:1 (2003), 9–10.
154. Storz, P., Döppler, H., Toker, A., Protein kinase Cδ selectively regulates protein kinase D-dependent activation of NF-κB in oxidative stress signaling. Mol. Cell. Biol. 24:7 (2004), 2614–2626.
155. Storz, P., Döppler, H., Toker, A., Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol. Cell. Biol. 25:19 (2005), 8520–8530.
156. Hruban, R.H., Iacobuzio-Donahue, C., Wilentz, R.E., Goggins, M., Kern, S.E., Molecular pathology of pancreatic cancer. Cancer J. 7:4 (2001), 251–258.
157. Kodydkova, J., Vavrova, L., Stankova, B., Macasek, J., Krechler, T., Zak, A., Antioxidant status and oxidative stress markers in pancreatic cancer and chronic pancreatitis. Pancreas 42:4 (2013), 614–621.
158. Liou, G.-Y., Döppler, H., DelGiorno, K.E., Zhang, L., Leitges, M., Crawford, H.C., Murphy, M.P., Storz, P., Mutant Kras-induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions. Cell Rep. 14:10 (2016), 2325–2336.
159. Singh, R., Czaja, M.J., Regulation of hepatocyte apoptosis by oxidative stress. J. Gastroenterol. Hepatol. 22 (2007), S45–S48.
160. Wang, Y., Schattenberg, J.M., Rigoli, R.M., Storz, P., Czaja, M.J., Hepatocyte resistance to oxidative stress is dependent on protein kinase C-mediated down-regulation of c-Jun/AP-1. J. Biol. Chem. 279:30 (2004), 31089–31097.
161. Chen, J., Deng, F., Singh, S.V., Wang, Q.J., Protein kinase D3 (PKD3) contributes to prostate cancer cell growth and survival through a PKCε/PKD3 pathway downstream of akt and ERK 1/2. Cancer Res. 68:10 (2008), 3844–3853.
162. Azoitei, N., Kleger, A., Schoo, N., Thal, D.R., Brunner, C., Pusapati, G.V., Filatova, A., Genze, F., Möller, P., Acker, T., Kuefer, R., Van Lint, J., Baust, H., Adler, G., Seufferlein, T., Protein kinase D2 is a novel regulator of glioblastoma growth and tumor formation. Neuro-oncology 13:7 (2011), 710–724.
163. Ahmed, K.M., Cao, N., Li, J.J., HER-2 and NF-κB as the targets for therapy-resistant Breast cancer. Anticancer Res. 26:0 (2006), 4235–4243.
164. Bourguignon, L.Y.W., Xia, W., Wong, G., Hyaluronan-mediated CD44 interaction with p300 and SIRT1 regulates β-Catenin signaling and NFκB-specific transcription activity leading to MDR1 and bcl-x(L) gene expression and chemoresistance in Breast tumor cells. J. Biol. Chem. 284:5 (2009), 2657–2671.
165. Duffey, D.C., Crowl-Bancroft, C.V., Chen, Z., Ondrey, F.G., Nejad-Sattari, M., Dong, G., Van Waes, C., Inhibition of transcription factor nuclear factor-κB by a mutant inhibitor-κβα attenuates resistance of human head and neck squamous cell carcinoma to TNF-α caspase-mediated cell death. Br. J. Cancer 83:10 (2000), 1367–1374.
166. Wang, Y., Huang, X., Cang, H., Gao, F., Yamamoto, T., Osaki, T., Yi, J., The endogenous reactive oxygen species promote NF-κβ activation by targeting on activation of NF-κB-inducing kinase in oral squamous carcinoma cells. Free Radic. Res. 41:9 (2007), 963–971.
167. No, J.H., Kim, Y.-B., Song, Y.S., Targeting Nrf2 signaling to combat chemoresistance. J. Cancer Prevent. 19:2 (2014), 111–117.
168. Padmanabhan, B., Tong, K.I., Ohta, T., Nakamura, Y., Scharlock, M., Ohtsuji, M., Kang, M.-I., Kobayashi, A., Yokoyama, S., Yamamoto, M., Structural basis for defects of keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21:5 (2006), 689–700.
169. Yoo, N.J., Kim, H.R., Kim, Y.R., An, C.H., Lee, S.H., Somatic mutations of the KEAP1 gene in common solid cancers. Histopathology 60:6 (2012), 943–952.
170. Kruiswijk, F., Labuschagne, C.F., Vousden, K.H., p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat. Rev. Mol. Cell Biol. 16:7 (2015), 393–405.
171. Levine, A.J., Oren, M., The first 30 years of p53: growing ever more complex. Nat. Rev. Cancer 9:10 (2009), 749–758.
172. Loeb, L.A., Loeb, K.R., Anderson, J.P., Multiple mutations and cancer. Proc. Natl. Acad. Sci. 100:3 (2003), 776–781.
173. Sieber, O.M., Heinimann, K., Tomlinson, I.P.M., Genomic instability [mdash] the engine of tumorigenesis?. Nat. Rev. Cancer 3:9 (2003), 701–708.
174. Karanjawala, Z.E., Murphy, N., Hinton, D.R., Hsieh, C.-L., Lieber, M.R., Oxygen metabolism causes chromosome Breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Curr. Biol. 12:5 (2002), 397–402.
175. Cooke, M.S., Evans, M.D., Dizdaroglu, M., Lunec, J., Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 17:10 (2003), 1195–1214.
176. Fan, J., Li, L., Small, D., Rassool, F., Cells expressing FLT3/ITD mutations exhibit elevated repair errors generated through alternative NHEJ pathways: implications for genomic instability and therapy. Blood 116:24 (2010), 5298–5305.
177. Skorski, T., BCR/ABL regulates response to DNA damage: the role in resistance to genotoxic treatment and in genomic instability. Oncogene 21:56 (2002), 8591–8604.
178. Skorski, T., Genomic instability: the cause and effect of BCR/ABL tyrosine kinase. Curr. Hematol. Malig. Rep. 2:2 (2007), 69–74.
179. Nowicki, M.O., Falinski, R., Koptyra, M., Slupianek, A., Stoklosa, T., Gloc, E., Nieborowska-Skorska, M., Blasiak, J., Skorski, T., BCR/ABL oncogenic kinase promotes unfaithful repair of the reactive oxygen species?dependent DNA double-strand breaks. Blood 104:12 (2004), 3746–3753.
180. Sallmyr, A., Fan, J., Rassool, F.V., Genomic instability in myeloid malignancies: increased reactive oxygen species (ROS), DNA double strand breaks (DSBs) and error-prone repair. Cancer Lett. 270:1 (2008), 1–9.
181. Dang, C.V., Semenza, G.L., Oncogenic alterations of metabolism. Trends Biochem. Sci. 24:2 (1999), 68–72.
182. Harris, A.L., Hypoxia [mdash] a key regulatory factor in tumour growth. Nat. Rev. Cancer 2:1 (2002), 38–47.
183. Dang, C.V., Links between metabolism and cancer. Genes. Dev. 26:9 (2012), 877–890.
184. 2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem. J. 418:1 (2009), 29–37.
185. Pani, G., Giannoni, E., Galeotti, T., Chiarugi, P., Redox-based escape mechanism from death: the cancer lesson. Antioxid. Redox Signal. 11:11 (2009), 2791–2806.
186. Chandel, N.S., McClintock, D.S., Feliciano, C.E., Wood, T.M., Melendez, J.A., Rodriguez, A.M., Schumacker, P.T., Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 Sensing. J. Biol. Chem. 275:33 (2000), 25130–25138.
187. Schroedl, C., McClintock, D.S., Budinger, G.R.S., Chandel, N.S., Hypoxic but not anoxic stabilization of HIF-1α requires mitochondrial reactive oxygen species. Am. J. Physiol.—Lung Cell. Mol. Physiol. 283:5 (2002), L922–L931.
188. Park, J.-H., Kim, T.-Y., Jong, H.-S., Kim, T.Y., Chun, Y.-S., Park, J.-W., Lee, C.-T., Jung, H.C., Kim, N.K., Bang, Y.-J., Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1α in gastric cancer cells. Clin. Cancer Res. 9:1 (2003), 433–440.
189. Ichijo, H., Nishida, E., Irie, K., Dijke, P.t., Saitoh, M., Moriguchi, T., Takagi, M., Matsumoto, K., Miyazono, K., Gotoh, Y., Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 5296:275 (1997), 90–94.
190. Moon, D.-O., Kim, M.-O., Choi, Y.H., Hyun, J.W., Chang, W.Y., Kim, G.-Y., Butein induces G2/M phase arrest and apoptosis in human hepatoma cancer cells through ROS generation. Cancer Lett. 288:2 (2010), 204–213.
191. Carmody, R.J., Cotter, T.G., Signalling apoptosis: a radical approach. Redox Rep. 6:2 (2001), 77–90.
192. Dhanasekaran, D.N., Reddy, E.P., JNK signaling in apoptosis. Oncogene 27:48 (2008), 6245–6251.
193. Pelicano, H., Feng, L., Zhou, Y., Carew, J.S., Hileman, E.O., Plunkett, W., Keating, M.J., Huang, P., Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem. 278:39 (2003), 37832–37839.
194. Sastre, J., Pallardó F.V., Viña, J., Mitochondrial oxidative stress plays a key role in aging and apoptosis. IUBMB Life 49:5 (2000), 427–435.
195. Kennedy, N.J., Davis, R.J., Role of JNK in tumor development. Cell cycle (Georgetown, Tex.) 2:3 (2003), 199–201.
196. Fulda, S., Debatin, K., Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25:34 (2006), 4798–4811.
197. Ashkenazi, A., Dixit, V.M., Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11:2 (1999), 255–260.
198. Berg, D., Lehne, M., Muller, N., Siegmund, D., Munkel, S., Sebald, W., Pfizenmaier, K., Wajant, H., Enforced covalent trimerization increases the activity of the TNF ligand family members TRAIL and CD95L. Cell Death Differ. 14:12 (2007), 2021–2034.
199. Yodkeeree, S., Sung, B., Limtrakul, P., Aggarwal, B.B., Zerumbone enhances TRAIL-induced apoptosis through the induction of death receptors in human colon cancer cells: evidence for an essential role of reactive oxygen species. Cancer Res. 69:16 (2009), 6581–6589.
200. + elevations and the mitochondrial permeability transition pore. J. Cell Sci. 115:3 (2002), 485–497.
201. Ryter, S.W., Kim, H.P., Hoetzel, A., Park, J.W., Nakahira, K., Wang, X., Choi, A.M., Mechanisms of cell death in oxidative stress. Antioxid. Redox Signal. 9:1 (2007), 49–89.
202. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Snow, B.E., Brothers, G.M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D.R., Aebersold, R., Siderovski, D.P., Penninger, J.M., Kroemer, G., Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:6718 (1999), 441–446.
203. Chen, Q., Lesnefsky, E.J., Depletion of cardiolipin and cytochrome c during ischemia increases hydrogen peroxide production from the electron transport chain. Free Radic. Biol. Med. 40:6 (2006), 976–982.
204. Kelekar, A., Thompson, C.B., Bcl-2-family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol. 8:8 (1998), 324–330.
205. Merad-Boudia, M., Nicole, A., Santiard-Baron, D., Saillé C., Ceballos-Picot, I., Mitochondrial impairment as an early event in the process of apoptosis induced by glutathione depletion in neuronal cells: relevance to Parkinson's disease. Biochem. Pharmacol. 56:5 (1998), 645–655.
206. Lu, C., Armstrong, J.S., Role of calcium and cyclophilin D in the regulation of mitochondrial permeabilization induced by glutathione depletion. Biochem. Biophys. Res. Commun. 363:3 (2007), 572–577.
207. D'Alessio, M., Cerella, C., De Nicola, M., Bergamaschi, A., Magrini, A., Gualandi, G., Alfonsi, A.M., Ghibelli, L., Apoptotic GSH extrusion is associated with free radical generation. Ann. N. Y. Acad. Sci. 1010:1 (2003), 449–452.
208. Poillet-Perez, L., Despouy, G., Delage-Mourroux, R., Boyer-Guittaut, M., Interplay between ROS and autophagy in cancer cells, from tumor initiation to cancer therapy. Redox Biol. 4 (2015), 184–192.
209. Li, L., Ishdorj, G., Gibson, S.B., Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic. Biol. Med. 53:7 (2012), 1399–1410.
210. Gibson, S.B., A matter of balance between life and death: targeting reactive oxygen species (ROS)-induced autophagy for cancer therapy. Autophagy 6:7 (2010), 835–837.
211. Azad, M.B., Chen, Y., Gibson, S.B., Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid. Redox Signal. 11:4 (2009), 777–790.
212. Maddocks, O.D.K., Vousden, K.H., Erratum to: metabolic regulation by p53. J. Mol. Med. (Berlin, Germany), 89(5), 2011, 531.
213. Tal, M.C., Sasai, M., Lee, H.K., Yordy, B., Shadel, G.S., Iwasaki, A., Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. 106:8 (2009), 2770–2775.
214. Quan, W., Lim, Y.-M., Lee, M.-S., Role of autophagy in diabetes and endoplasmic reticulum stress of pancreatic [beta]-cells. Exp. Mol. Med. 44 (2012), 81–88.
215. Morselli, E., Galluzzi, L., Kepp, O., Vicencio, J.-M., Criollo, A., Maiuri, M.C., Kroemer, G., Anti- and pro-tumor functions of autophagy. Biochim. Biophys. Acta (BBA) − Mol. Cell Res. 1793:9 (2009), 1524–1532.
216. Debnath, J., The multifaceted roles of autophagy In Tumors?Implications for Breast cancer. J. Mammary Gland Biol. Neoplasia 16:3 (2011), 173–187.
217. Zhang, J., Ney, P.A., Role of BNIP3 and nix in cell death, autophagy, and, mitophagy. Cell Death Differ. 16:7 (2009), 939–946.
218. Novak, I., Mitophagy: a complex mechanism of mitochondrial removal. Antioxid. Redox Signal. 17:5 (2012), 794–802.
219. Feng, D., Liu, L., Zhu, Y., Chen, Q., Molecular signaling toward mitophagy and its physiological significance. Exp. Cell Res. 319:12 (2013), 1697–1705.
220. Youle, R.J., Narendra, D.P., Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12:1 (2011), 9–14.
221. Matsuda, N., Sato, S., Shiba, K., Okatsu, K., Saisho, K., Gautier, C.A., Sou, Y.-s., Saiki, S., Kawajiri, S., Sato, F., Kimura, M., Komatsu, M., Hattori, N., Tanaka, K., PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 189:2 (2010), 211–221.
222. Morselli, E., Galluzzi, L., Kepp, O., Mariño, G., Michaud, M., Vitale, I., Maiuri, M.C., Kroemer, G., Oncosuppressive functions of autophagy. Antioxid. Redox Signal. 14:11 (2010), 2251–2269.
223. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y.-S., Ueno, I., Sakamoto, A., Tong, K.I., Kim, M., Nishito, Y., Iemura, S.-i., Natsume, T., Ueno, T., Kominami, E., Motohashi, H., Tanaka, K., Yamamoto, M., The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12:3 (2010), 213–223.
224. Lau, A., Wang, X.-J., Zhao, F., Villeneuve, N.F., Wu, T., Jiang, T., Sun, Z., White, E., Zhang, D.D., A noncanonical mechanism of nrf2 activation by autophagy deficiency: direct interaction between keap1 and p62. Mol. Cell. Biol. 30:13 (2010), 3275–3285.
225. Taguchi, K., Fujikawa, N., Komatsu, M., Ishii, T., Unno, M., Akaike, T., Motohashi, H., Yamamoto, M., Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc. Natl. Acad. Sci. 109:34 (2012), 13561–13566.
226. Villeneuve, N.F., Lau, A., Zhang, D.D., Regulation of the Nrf2–Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid. Redox Signal. 13:11 (2010), 1699–1712.
227. Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K., Mizushima, N., Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 25:8 (2011), 795–800.
228. Mathew, R., Kongara, S., Beaudoin, B., Karp, C.M., Bray, K., Degenhardt, K., Chen, G., Jin, S., White, E., Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21:11 (2007), 1367–1381.
229. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S., White, E., Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21:13 (2007), 1621–1635.
230. Aita, V.M., Liang, X.H., V.V.V.S, Murty, Pincus, D.L., Yu, W., Cayanis, E., Kalachikov, S., Gilliam, T.C., Levine, B., Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59:1 (1999), 59–65.
231. Choi, A.M.K., Ryter, S.W., Levine, B., Autophagy in human health and disease. New Engl. J. Med. 368:7 (2013), 651–662.
232. Liang, X.H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., Levine, B., Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:6762 (1999), 672–676.
233. Laddha, S.V., Ganesan, S., Chan, C.S., White, E., Mutational landscape of the essential autophagy gene BECN1 in human cancers. Mol. Cancer Res.: MCR 12:4 (2014), 485–490.
234. Guo, J.Y., Chen, H.-Y., Mathew, R., Fan, J., Strohecker, A.M., Karsli-Uzunbas, G., Kamphorst, J.J., Chen, G., Lemons, J.M.S., Karantza, V., Coller, H.A., DiPaola, R.S., Gelinas, C., Rabinowitz, J.D., White, E., Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25:5 (2011), 460–470.
235. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J.M., Dell'Antonio, G., Mautner, J., Tonon, G., Haigis, M., Shirihai, O.S., Doglioni, C., Bardeesy, N., Kimmelman, A.C., Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25:7 (2011), 717–729.
236. Kim, M.-J., Woo, S.-J., Yoon, C.-H., Lee, J.-S., An, S., Choi, Y.-H., Hwang, S.-G., Yoon, G., Lee, S.-J., Involvement of autophagy in oncogenic K-Ras-induced malignant cell transformation. J. Biol. Chem. 286:15 (2011), 12924–12932.
237. Xu, R.-H., Pelicano, H., Zhou, Y., Carew, J.S., Feng, L., Bhalla, K.N., Keating, M.J., Huang, P., Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res. 65:2 (2005), 613–621.
238. Brown, J.M., Wilson, W.R., Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4:6 (2004), 437–447.
239. Erler, J.T., Cawthorne, C.J., Williams, K.J., Koritzinsky, M., Wouters, B.G., Wilson, C., Miller, C., Demonacos, C., Stratford, I.J., Dive, C., Hypoxia-Mediated down-Regulation of bid and bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance. Mol. Cell. Biol. 24:7 (2004), 2875–2889.
240. Moeller, B.J., Cao, Y., Li, C.Y., Dewhirst, M.W., Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5:5 (2004), 429–441.
241. Unruh, A., Ressel, A., Mohamed, H.G., Johnson, R.S., Nadrowitz, R., Richter, E., Katschinski, D.M., Wenger, R.H., The hypoxia-inducible factor-1[alpha] is a negative factor for tumor therapy. Oncogene 22:21 (2003), 3213–3220.
242. Goodman, J., Hochstein, P., Generation of free radicals and lipid peroxidation by redox cycling of adriamycin and daunomycin. Biochem. Biophys. Res. Commun. 77:2 (1977), 797–803.
243. Doroshow, J.H., Anthracycline antibiotic-stimulated superoxide, hydrogen peroxide, and hydroxyl radical production by NADH dehydrogenase. Cancer Res. 43:10 (1983), 4543–4551.
244. Pan, S.-S., Pedersen, L., Bachur, N.R., Comparative flavoprotein catalysis of anthracycline antibiotic. Reduc. Cleav. Oxygen Consump. 19:1 (1981), 184–186.
245. Bachur, N.R., Gordon, S.L., Gee, M.V., Anthracycline antibiotic augmentation of microsomal electron transport and free radical formation. Mol. Pharmacol. 13:5 (1977), 901–910.
246. Bates, D.A., Winterbourn, C.C., Deoxyribose breakdown by the adriamycin semiquinone and H2O2: evidence for hydroxyl radical participation. FEBS Lett. 145:1 (1982), 137–142.
247. Bachur, N.R., Gordon, S.L., Gee, M.V., A general mechanism for microsomal activation of quinone anticancer agents to free radicals. Cancer Res. 38:6 (1978), 1745–1750.
248. Sinha, B.K., Free radicals in anticancer drug pharmacology. Chem. Biol. Interact. 69:4 (1989), 293–317.
249. Bustamante, J., Galleano, M., Medrano, E.E., Boveris, A., Adriamycin effects on hydroperoxide metabolism and growth of human breast tumor cells. Breast Cancer Res. Treat. 17:2 (1990), 145–153.
250. Benchekroun, M.N., Sinha, B.K., Robert, J., Doxorubicin-induced oxygen free radical formation in sensitive and doxorubicin-resistant variants of rat glioblastoma cell lines. FEBS Lett. 322:3 (1993), 295–298.
251. Serrano, J., Palmeira, C.M., Kuehl, D.W., Wallace, K.B., Cardioselective and cumulative oxidation of mitochondrial DNA following subchronic doxorubicin administration1. Biochim. Biophys. Acta (BBA)—Bioenergetics 1411:1 (1999), 201–205.
252. Mas, V.M.-D., Bezombes, C., Quillet-Mary, A., Bettaïeb, A., D'orgeix, A.D.T., Laurent, G., Jaffrézou, J.-P., Implication of radical oxygen species in ceramide generation, c-Jun N-terminal kinase activation and apoptosis induced by daunorubicin. Mol. Pharmacol. 56:5 (1999), 867–874.
253. Gouazé V., Mirault, M.-E., Carpentier, S., Salvayre, R., Levade, T., Andrieu-Abadie, N., Glutathione peroxidase-1 overexpression prevents ceramide production and partially inhibits apoptosis in doxorubicin-treated human Breast carcinoma cells. Mol. Pharmacol. 60:3 (2001), 488–496.
254. Singal, P.K., Iliskovic, N., Doxorubicin-Induced cardiomyopathy. New Engl. J. Med. 39:13 (1998), 900–905.
255. Buzdar, A.U., Marcus, C., Blumenschein, G.R., Smith, T.L., Early and delayed clinical cardiotoxicity of doxorubicin. Cancer 55:12 (1985), 2761–2765.
256. Wang, S., Konorev, E.A., Kotamraju, S., Joseph, J., Kalivendi, S., Kalyanaraman, B., Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms: intermediacy of H2O2- and p53-dependent pathways. J. Biol. Chem. 279:24 (2004), 25535–25543.
257. Lowe, S., Bodis, S., McClatchey, A., Remington, L., Ruley, H., Fisher, D., Housman, D., Jacks, T., p53 status and the efficacy of cancer therapy in vivo. Science 266:5186 (1994), 807–810.
258. Lotem, J., Peled-Kamar, M., Groner, Y., Sachs, L., Cellular oxidative stress and the control of apoptosis by wild-type p53, cytotoxic compounds, and cytokines. Proc. Natl. Acad. Sci. 93:17 (1996), 9166–9171.
259. Holley, A.K., Miao, L., St. Clair, D.K., St. Clair, W.H., Redox-modulated phenomena and radiation therapy the central role of superoxide dismutases. Antioxid. Redox Signal. 20:10 (2014), 1567–1589.
260. Baskar, R., Lee, K.A., Yeo, R., Yeoh, K.-W., Cancer and radiation therapy: current advances and future directions. Int. J. Med. Sci. 9:3 (2012), 193–199.
261. Delaney, G., Jacob, S., Featherstone, C., Barton, M., The role of radiotherapy in cancer treatment. Cancer 104:6 (2005), 1129–1137.
262. Marchetti, M., Resnick, L., Gamliel, E., Kesaraju, S., Weissbach, H., Binninger, D., Sulindac enhances the killing of cancer cells exposed to oxidative stress. PLoS One, 4(6), 2009, e5804.
263. Vaughn, A.E., Deshmukh, M., Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10:12 (2008), 1477–1483.
264. Ahmad, I.M., Abdalla, M.Y., Aykin-Burns, N., Simons, A.L., Oberley, L.W., Domann, F.E., Spitz, D.R., 2-Deoxyglucose combined with wild-type p53 overexpression enhances cytotoxicity in human prostate cancer cells via oxidative stress. Free Radic. Biol. Med. 44:5 (2008), 826–834.
265. Coleman, M.C., Asbury, C.R., Daniels, D., Du, J., Aykin-Burns, N., Smith, B.J., Li, L., Spitz, D.R., Cullen, J.J., 2-Deoxy-d-glucose causes cytotoxicity, oxidative stress, and radiosensitization in pancreatic cancer. Free Radic. Biol. Med. 44:3 (2008), 322–331.
266. Russell, E.G., O'Sullivan, E.C., Miller, C.M., Stanicka, J., McCarthy, F.O., Cotter, T.G., Ellipticine derivative induces potent cytostatic effect in acute myeloid leukaemia cells. Invest. New Drugs 32:6 (2014), 1113–1122.
267. Russell, E.G., Guo, J., O'Sullivan, E.C., O'Driscoll, C.M., McCarthy, F.O., Cotter, T.G., 7-formyl-10-methylisoellipticine, a novel ellipticine derivative, induces mitochondrial reactive oxygen species (ROS) and shows anti-leukaemic activity in mice. Invest. New Drugs 34:1 (2016), 15–23.
268. El-Mir, M.-Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M., Leverve, X., Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 275:1 (2000), 223–228.
269. Owen, M.R., Doran, E., Halestrap, A.P., Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem. J. 348:Pt 3 (2000), 607–614.
270. Wheaton, W.W., Weinberg, S.E., Hamanaka, R.B., Soberanes, S., Sullivan, L.B., Anso, E., Glasauer, A., Dufour, E., Mutlu, G.M., Budigner, G.R.S., Chandel, N.S., Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis. eLife, 3, 2014, e02242.
271. Noto, H., Goto, A., Tsujimoto, T., Noda, M., Cancer risk in diabetic patients treated with metformin: a systematic review and meta-analysis. PLoS One, 7(3), 2012, e33411.
272. Cheng, G., Lanza-Jacoby, S., Metformin decreases growth of pancreatic cancer cells by decreasing reactive oxygen species: role of NOX4. Biochem. Biophys. Res. Commun. 465:1 (2015), 41–46.
273. Mochizuki, T., Furuta, S., Mitsushita, J., Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 25:26 (2006), 3699–3707.
274. Teoh-Fitzgerald, M.L., Fitzgerald, M.P., Zhong, W., Askeland, R.W., Domann, F.E., Epigenetic reprogramming governs EcSOD expression during human mammary epithelial cell differentiation, tumorigenesis and metastasis. Oncogene 33:3 (2014), 358–368.
275. Omenn, G.S., Goodman, M.D., Thornquist, J., Balmes, M.R., Cullen, A., Glass, J.P., Keogh, F.L.J., Meyskens, B., Valanis, J.H.J., Williams, S., Hammar, S., Effects of a combination of beta carotene and vitamin a on lung cancer and cardiovascular disease. New Engl. J. Med. 334:18 (1996), 1150–1155.
276. Klein, E.A., Thompson, I.M., Tangen, C.M., Crowley, J.J., Lucia, M.S., Goodman, P.J., Minasian, L., Ford, L.G., Parnes, H.L., Gaziano, J.M., Karp, D.D., Lieber, M.M., Walther, P.J., Klotz, L., Parsons, J.K., Chin, J.L., Darke, A.K., Lippman, S.M., Goodman, G.E., Meyskens, F.L., Baker, L.H., Vitamin e and the risk of prostate cancer: updated results of the selenium and vitamin e cancer prevention trial (SELECT). JAMA 306:14 (2011), 1549–1556.