NADPH oxidase 1 supports proliferation of colon cancer cells by modulating reactive oxygen species-dependent signal transduction

Journal of Biological Chemistry

Volumn 292, Issue 19, 2017, Pages 7866-7887

  Juhasz, Agnes ^a   Markel, Susan ^b   Gaur, Shikha ^b   Liu, Han ^a   Lu, Jiamo ^a   Jiang, Guojian ^a   Wu, Xiwei ^b   Antony, Smitha ^a   Wu, Yongzhong ^a   Melillo, Giovanni ^c   Meitzler, Jennifer L ^a   Haines, Diana C ^d   Butcher, Donna ^d   Roy, Krishnendu ^a   Doroshow, James H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c SAIC FREDERICK INC   (United States)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; BLOOD VESSELS; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CELLS; CYTOLOGY; DISEASES; POLYMERASE CHAIN REACTION; PROTEINS; SIGNAL TRANSDUCTION;

HUMAN COLON CANCER CELLS; HYPOXIA INDUCIBLE FACTOR 1-ALPHA; MICROARRAY ANALYSIS; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN EXPRESSIONS; PROTEIN PHOSPHATASE; REACTIVE OXYGEN SPECIES; THERAPEUTIC TARGETS;

CELL SIGNALING;

CYCLIN D1; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; OXIDOREDUCTASE; RAF PROTEIN; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SHORT HAIRPIN RNA; VASCULOTROPIN; CCND1 PROTEIN, HUMAN; CD31 ANTIGEN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NOX1 PROTEIN, HUMAN; SMALL INTERFERING RNA; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CELL PROLIFERATION; COLON CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; ONCOGENE C MYB; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; S PHASE CELL CYCLE CHECKPOINT; SIGNAL TRANSDUCTION; STEADY STATE; TUMOR GROWTH; WESTERN BLOTTING; XENOGRAFT; ANIMAL; CANCER TRANSPLANTATION; CELL CYCLE; COLON; COLON TUMOR; GENE EXPRESSION REGULATION; HT-29 CELL LINE; MALE; METABOLISM; MOUSE; PHOSPHORYLATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD31; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; COLON; COLONIC NEOPLASMS; CYCLIN D1; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MAP KINASE SIGNALING SYSTEM; MICE; NADPH OXIDASE; NEOPLASM TRANSPLANTATION; PHENOTYPE; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85019408389     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.768283     Document Type: Article

References (76)

1. Dröge, W. (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95
2. Nathan, C. (2003) Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J. Clin. Invest. 111, 769-778
3. Rhee, S. G. (2006) Cell signaling. H2O2, a necessary evil for cell signaling. Science 312, 1882-1883
4. Burdon, R. H. (1995) Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 18, 775-794
5. Sablina, A. A., Budanov, A. V., Ilyinskaya, G. V., Agapova, L. S., Kravchenko, J. E., and Chumakov, P. M. (2005) The antioxidant function of the p53 tumor suppressor. Nat. Med. 11, 1306-1313
6. Kuroki, M., Voest, E. E., Amano, S., Beerepoot, L. V., Takashima, S., Tolentino, M., Kim, R. Y., Rohan, R. M., Colby, K. A., Yeo, K. T., and Adamis, A. P. (1996) Reactive oxygen intermediates increase vascular endothelial growth factor expression in vitro and in vivo. J. Clin. Invest. 98, 1667-1675
7. Arbiser, J. L., Petros, J., Klafter, R., Govindajaran, B., McLaughlin, E. R., Brown, L. F., Cohen, C., Moses, M., Kilroy, S., Arnold, R. S., and Lambeth, J. D. (2002) Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc. Natl. Acad. Sci. U.S.A. 99, 715-720
8. 2-induced, ERK-associated up-regulation of HIF-1α and VEGF-A. Oncotarget 7, 68412-68433
9. Okada, F., Kobayashi, M., Tanaka, H., Kobayashi, T., Tazawa, H., Iuchi, Y., Onuma, K., Hosokawa, M., Dinauer, M. C., and Hunt, N. H. (2006) The role of nicotinamide adenine dinucleotide phosphate oxidase-derived reactive oxygen species in the acquisition of metastatic ability of tumor cells. Am. J. Pathol. 169, 294-302
10. Doroshow, J. H. (2006) Redox modulation of chemotherapy-induced tumor cell killing and normal tissue toxicity. J. Natl. Cancer Inst. 98, 223-225
11. Chiera, F., Meccia, E., Degan, P., Aquilina, G., Pietraforte, D., Minetti, M., Lambeth, D., and Bignami, M. (2008) Overexpression of human NOX1 complex induces genome instability in mammalian cells. Free Radic. Biol. Med. 44, 332-342
12. Szatrowski, T. P., and Nathan, C. F. (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51, 794-798
13. Soares, F. A., Shaughnessy, S. G., MacLarkey, W. R., and Orr, F. W. (1994) Quantification and morphologic demonstration of reactive oxygen species produced by Walker 256 tumor cells in vitro and during metastasis in vivo. Lab. Invest. 71, 480-489
14. Lambeth, J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nature Rev. Immun. 4, 181-189
15. Babior, B. M., Lambeth, J. D., and Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344
16. Bedard, K., and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
17. Roy, K., Wu, Y., Meitzler, J. L., Juhasz, A., Liu, H., Jiang, G., Lu, J., Antony, S., and Doroshow, J. H. (2015) NADPH oxidases and cancer. Clin. Sci. 128, 863-875
18. Suh, Y.-A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K., and Lambeth, J. D. (1999) Cell transformation by the superoxide-generating oxidase Mox1. Nature 401, 79-82
19. Geiszt, M. (2006) NADPH oxidases: new kids on the block. Cardiovasc. Res. 71, 289-299
20. Lambeth, J. D., Cheng, G., Arnold, R. S., and Edens, W. A. (2000) Novel homologs of gp91phox. Trends Biochem. Sci. 25, 459-461
21. Bánfi, B., Clark, R. A., Steger, K., and Krause, K. H. (2003) Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 278, 3510-3513
22. Cheng, G., and Lambeth, J. D. (2004) NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J. Biol. Chem. 279, 4737-4742
23. Ambasta, R. K., Kumar, P., Griendling, K. K., Schmidt, H. H., Busse, R., and Brandes, R. P. (2004) Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279, 45935-45941
24. Sharma, P., Chakraborty, R., Wang, L., Min, B., Tremblay, M. L., Kawahara, T., Lambeth, J. D., and Haque, S. J. (2008) Redox regulation of interleukin-4 signaling. Immunity 29, 551-564
25. Mouzaoui, S., Djerdjouri, B., Makhezer, N., Kroviarski, Y., El-Benna, J., and Dang, P. M. (2014) Tumor necrosis factor-α-induced colitis increases NADPH oxidase 1 expression, oxidative stress, and neutrophil recruitment in the colon: preventive effect of apocyanin. Mediators Inflamm. 2014, 312484
26. Esworthy, R. S., Kim, B. W., Chow, J., Shen, B., Doroshow, J. H., and Chu, F. F. (2014) Nox1 causes ileocolitis in mice deficient in glutathione peroxidase-1 and -2. Free Radic. Biol. Med. 68, 315-325
27. Geiszt, M., Lekstrom, K., Brenner, S., Hewitt, S. M., Dana, R., Malech, H. L., and Leto, T. L. (2003) NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J. Immunol. 171, 299-306
28. Beaugerie, L., and Itzkowitz, S. H. (2015) Cancers complicating inflammatory bowel disease. N. Engl. J. Med. 372, 1441-1452
29. MacFie, T. S., Poulsom, R., Parker, A., Warnes, G., Boitsova, T., Nijhuis, A., Suraweera, N., Poehlmann, A., Szary, J., Feakins, R., Jeffery, R., Harper, R. W., Jubb, A. M., Lindsay, J. O., and Silver, A. (2014) DUOX2 and DUOXA2 form the predominant enzyme system capable of producing the reactive oxygen species H2O2 in active ulcerative colitis and are modulated by 5-aminosalicylic acid. Inflamm. Bowel Dis. 20, 514-524
30. Laurent, E., McCoy, J. W., 3rd., Macina, R. A., Liu, W., Cheng, G., Robine, S., Papkoff, J., and Lambeth, J. D. (2008) Nox1 is over-expressed in human colon cancers and correlates with activating mutations in K-Ras. Int. J. Cancer 123, 100-107
31. Juhasz, A., Ge, Y., Markel, S., Chiu, A., Matsumoto, L., van Balgooy, J., Roy, K., and Doroshow, J. H. (2009) Expression of NADPH oxidase homologues and accessory genes in human cancer cell lines, tumours and adjacent normal tissues. Free Radic. Res. 43, 523-532
32. Kawahara, T., Kuwano, Y., Teshima-Kondo, S., Takeya, R., Sumimoto, H., Kishi, K., Tsunawaki, S., Hirayama, T., and Rokutan, K. (2004) Role of nicotinamide adenine dinucleotide phosphate oxidase 1 in oxidative burst response to Toll-like receptor 5 signaling in large intestinal epithelial cells. J. Immunol. 172, 3051-3058
33. Teshima, S., Kutsumi, H., Kawahara, T., Kishi, K., and Rokutan, K. (2000) Regulation of growth and apoptosis of cultured guinea pig gastric mucosal cells by mitogenic oxidase 1. Am. J. Physiol. Gastrointest. Liver Physiol 279, G1169-G1176
34. Chamulitrat, W., Schmidt, R., Tomakidi, P., Stremmel, W., Chunglok, W., Kawahara, T., and Rokutan, K. (2003) Association of gp91phox homolog Nox1 with anchorage-independent growth and MAP kinase-activation of transformed human keratinocytes. Oncogene 22, 6045-6053
35. Mitsushita, J., Lambeth, J. D., and Kamata, T. (2004) The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res. 64, 3580-3585
36. Creighton-Gutteridge, M., Cardellina, J. H., 2nd., Stephen, A. G., Rapisarda, A., Uranchimeg, B., Hite, K., Denny, W. A., Shoemaker, R. H., and Melillo, G. (2007) Cell type-specific, topoisomerase II-dependent inhibition of hypoxia-inducible factor-1α protein accumulation by NSC 644221. Clin. Cancer Res. 13, 1010-1018
37. Coant, N., Ben Mkaddem, S., Pedruzzi, E., Guichard, C., Tréton, X., Ducroc, R., Freund, J. N., Cazals-Hatem, D., Bouhnik, Y., Woerther, P. L., Skurnik, D., Grodet, A., Fay, M., Biard, D., Lesuffleur, T., et al. (2010) NADPH oxidase 1 modulates WNT and NOTCH1 signaling to control the fate of proliferative progenitor cells in the colon. Mol. Cell. Biol. 30, 2636-2650
38. Garrido-Urbani, S., Jemelin, S., Deffert, C., Carnesecchi, S., Basset, O., Szyndralewiez, C., Heitz, F., Page, P., Montet, X., Michalik, L., Arbiser, J., Rüegg, C., Krause, K. H., Imhof, B. A., and Imhof, B. (2011) Targeting vascular NADPH oxidase 1 blocks tumor angiogenesis through a PPARα mediated mechanism. PLoS One 6, e14665
39. Wang, R., Dashwood, W. M., Nian, H., Löhr, C. V., Fischer, K. A., Tsuchiya, N., Nakagama, H., Ashktorab, H., and Dashwood, R. H. (2011) NADPH oxidase overexpression in human colon cancers and rat colon tumors induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Int. J. Cancer 128, 2581-2590
40. Doroshow, J. H., Juhasz, A., Ge, Y., Holbeck, S., Lu, J., Antony, S., Wu, Y., Jiang, G., and Roy, K. (2012) Antiproliferative mechanisms of action of the flavin dehydrogenase inhibitors diphenylene iodonium and di-2-thienyliodonium based on molecular profiling of the NCI-60 human tumor cell panel. Biochem. Pharmacol. 83, 1195-1207
41. Cheng, G., Diebold, B. A., Hughes, Y., and Lambeth, J. D. (2006) Nox1-dependent reactive oxygen generation is regulated by Rac1. J. Biol. Chem. 281, 17718-17726
42. Cross, J. V., and Templeton, D. J. (2006) Regulation of signal transduction through protein cysteine oxidation. Antioxid. Redox Signal. 8, 1819-1827
43. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54
44. Knowles, H. J., Raval, R. R., Harris, A. L., and Ratcliffe, P. J. (2003) Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res. 63, 1764-1768
45. Kietzmann, T., and Görlach, A. (2005) Reactive oxygen species in the control of hypoxia-inducible factor-mediated gene expression. Semin. Cell Dev. Biol. 16, 474-486
46. Block, K., Gorin, Y., Hoover, P., Williams, P., Chelmicki, T., Clark, R. A., Yoneda, T., and Abboud, H. E. (2007) NAD(P)H Oxidases regulate HIF-2 α protein expression. J. Biol. Chem. 282, 8019-8026
47. Leto, T. L., and Geiszt, M. (2006) Role of Nox family NADPH oxidases in host defense. Antioxid. Redox Signal. 8, 1549-1561
48. Arnold, R. S., Shi, J., Murad, E., Whalen, A. M., Sun, C. Q., Polavarapu, R., Parthasarathy, S., Petros, J. A., and Lambeth, J. D. (2001) Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase nox1. Proc. Natl. Acad. Sci. U.S.A. 98, 5550-5555
49. Preston, T. J., Muller, W. J., and Singh, G. (2001) Scavenging of extracellular H2O2 by catalase inhibits the proliferation of HER-2/Neu-transformed rat-1 fibroblasts through the induction of a stress response. J. Biol. Chem. 276, 9558-9564
50. Menon, S. G., Sarsour, E. H., Spitz, D. R., Higashikubo, R., Sturm, M., Zhang, H., and Goswami, P. C. (2003) Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle. Cancer Res. 63, 2109-2117
51. Arnold, R. S., He, J., Remo, A., Ritsick, D., Yin-Goen, Q., Lambeth, J. D., Datta, M. W., Young, A. N., and Petros, J. A. (2007) Nox1 expression determines cellular reactive oxygen and modulates c-fos-induced growth factor, interleukin-8, and Cav-1. Am. J. Pathol. 171, 2021-2032
52. Menon, S. G., and Goswami, P. C. (2007) A redox cycle within the cell cycle: ring in the old with the new. Oncogene 26, 1101-1109
53. Venkatachalam, P., de Toledo, S. M., Pandey, B. N., Tephly, L. A., Carter, A. B., Little, J. B., Spitz, D. R., and Azzam, E. I. (2008) Regulation of normal cell cycle progression by flavin-containing oxidases. Oncogene 27, 20-31
54. Cánepa, E. T., Scassa, M. E., Ceruti, J. M., Marazita, M. C., Carcagno, A. L., Sirkin, P. F., and Ogara, M. F. (2007) INK4 proteins, a family of mammalian CDK inhibitors with novel biological functions. IUBMB Life 59, 419-426
55. Xing, J., Ginty, D. D., and Greenberg, M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963
56. Fox, K. E., Colton, L. A., Erickson, P. F., Friedman, J. E., Cha, H. C., Keller, P., MacDougald, O. A., and Klemm, D. J. (2008) Regulation of cyclin D1 and Wnt10b gene expression by cAMP-responsive element-binding protein during early adipogenesis involves differential promoter methylation. J. Biol. Chem. 283, 35096-35105
57. Sée, V., and Loeffler, J. P. (2001) Oxidative stress induces neuronal death by recruiting a protease and phosphatase-gated mechanism. J. Biol. Chem. 276, 35049-35059
58. Bedogni, B., Pani, G., Colavitti, R., Riccio, A., Borrello, S., Murphy, M., Smith, R., Eboli, M. L., and Galeotti, T. (2003) Redox regulation of cAMP-responsive element-binding protein and induction of manganous superoxide dismutase in nerve growth factor-dependent cell survival. J. Biol. Chem. 278, 16510-16519
59. Knebel, A., Rahmsdorf, H. J., Ullrich, A., and Herrlich, P. (1996) Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J. 15, 5314-5325
60. Ostman, A., Hellberg, C., and Böhmer, F. D. (2006) Protein-tyrosine phosphatases and cancer. Nat. Rev. Cancer 6, 307-320
61. Ahn, J. H., and Lee, M. (2008) Tyrosine phosphorylation and Ras activation is required for hydrogen peroxide-mediated Raf-1 kinase activation. Mol. Cell. Biochem. 317, 121-129
62. von Kriegsheim, A., Pitt, A., Grindlay, G. J., Kolch, W., and Dhillon, A. S. (2006) Regulation of the Raf-MEK-ERK pathway by protein phosphatase 5. Nat. Cell Biol. 8, 1011-1016
63. Li, B. H., Yang, X. Z., Li, P. D., Yuan, Q., Liu, X. H., Yuan, J., and Zhang, W. J. (2008) IL-4/Stat6 activities correlate with apoptosis and metastasis in colon cancer cells. Biochem. Biophys. Res. Commun. 369, 554-560
64. Doroshow, J. H., Gaur, S., Markel, S., Lu, J., van Balgooy, J., Synold, T. W., Xi, B., Wu, X., and Juhasz, A. (2013) Effects of iodonium-class flavin dehydrogenase inhibitors on growth, reactive oxygen production, cell cycle progression, NADPH oxidase 1 levels, and gene expression in human colon cancer cells and xenografts. Free Radic. Biol. Med. 57, 162-175
65. Honoré, S., Kovacic, H., Pichard, V., Briand, C., and Rognoni, J. B. (2003) α2β1-integrin signaling by itself controls G1/S transition in a human adenocarcinoma cell line (Caco-2): implication of NADPH oxidase-dependent production of ROS. Exp. Cell Res. 285, 59-71
66. Sadok, A., Bourgarel-Rey, V., Gattacceca, F., Penel, C., Lehmann, M., and Kovacic, H. (2008) Nox1-dependent superoxide production controls colon adenocarcinoma cell migration. Biochim. Biophys. Acta 1783, 23-33
67. Qiu, J., Ai, L., Ramachandran, C., Yao, B., Gopalakrishnan, S., Fields, C. R., Delmas, A. L., Dyer, L. M., Melnick, S. J., Yachnis, A. T., Schwartz, P. H., Fine, H. A., Brown, K. D., and Robertson, K. D. (2008) Invasion suppressor cystatin E/M (CST6): high-level cell type-specific expression in normal brain and epigenetic silencing in gliomas. Lab. Invest. 88, 910-925
68. Ramsay, R. G., and Gonda, T. J. (2008) MYB function in normal and cancer cells. Nat. Rev. Cancer 8, 523-534
69. Wolf, G., Hannken, T., Schroeder, R., Zahner, G., Ziyadeh, F. N., and Stahl, R. A. (2001) Antioxidant treatment induces transcription and expression of transforming growth factor β in cultured renal proximal tubular cells. FEBS Lett. 488, 154-159
70. Nikitenko, L. L., Fox, S. B., Kehoe, S., Rees, M. C., and Bicknell, R. (2006) Adrenomedullin and tumour angiogenesis. Br. J. Cancer 94, 1-7
71. Phillips, R. J., Mestas, J., Gharaee-Kermani, M., Burdick, M. D., Sica, A., Belperio, J. A., Keane, M. P., and Strieter, R. M. (2005) Epidermal growth factor and hypoxia-induced expression of CXC chemokine receptor 4 on non-small cell lung cancer cells is regulated by the phosphatidylinositol 3-kinase/PTEN/AKT/mammalian target of rapamycin signaling pathway and activation of hypoxia inducible factor-1α. J. Biol. Chem. 280, 22473-22481
72. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
73. Lee, N. S., Dohjima, T., Bauer, G., Li, H., Li, M. J., Ehsani, A., Salvaterra, P., and Rossi, J. (2002) Expression of small interfering RNAs targeted against HIV-1 rev transcripts in human cells. Nat. Biotechnol. 20, 500-505
74. Castanotto, D., Li, H., and Rossi, J. J. (2002) Functional siRNA expression from transfected PCR products. RNA 8, 1454-1460
75. Nisimoto, Y., Tsubouchi, R., Diebold, B. A., Qiao, S., Ogawa, H., Ohara, T., and Tamura, M. (2008) Activation of NADPH oxidase 1 in tumour colon epithelial cells. Biochem. J. 415, 57-65
76. Wu, Y., Antony, S., Juhasz, A., Lu, J., Ge, Y., Jiang, G., Roy, K., and Doroshow, J. H. (2011) Up-regulation and sustained activation of Stat1 are essential for interferon-γ (IFN-γ)-induced dual oxidase 2 (Duox2) and dual oxidase A2 (DuoxA2) expression in human pancreatic cancer cell lines. J. Biol. Chem. 286, 12245-12256