Diphenylene iodonium interferes with cell cycle progression and induces apoptosis by modulating NAD(P)H oxidase/ROS/cell cycle regulatory pathways in Burkitt's lymphoma cells

Oncology Reports

Volumn 33, Issue 3, 2015, Pages 1434-1442

  Ding, Ya ^a   Zhu, Wenjun ^b   Sun, Rui ^a   Yuan, Gang ^b   Zhang, Dongsheng ^a   Fan, Yuhua ^b   Sun, Jian ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Cell cycle; Diphenylene iodonium; Raji BL cells; ROS

Indexed keywords

CELL PROTEIN; DIPHENYLIODONIUM SALT; LACTIC ACID; LATENT MEMBRANE PROTEIN 1; MYC PROTEIN; PROTEIN CDC25A; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG; CATION; CDC25A PROTEIN, HUMAN; EBV-ASSOCIATED MEMBRANE ANTIGEN, EPSTEIN-BARR VIRUS; MATRIX PROTEIN; MYC PROTEIN, HUMAN; PROTEIN TYROSINE PHOSPHATASE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; EPSTEIN BARR VIRUS INFECTION; FLOW CYTOMETRY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IMMUNOBLOTTING; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAJI CELL LINE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS CELL INTERACTION; BIOSYNTHESIS; CELL SURVIVAL; DRUG EFFECTS; EPSTEIN BARR VIRUS; GENETICS; M PHASE CELL CYCLE CHECKPOINT; METABOLISM; PATHOGENICITY; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; VIROLOGY;

APOPTOSIS; BURKITT LYMPHOMA; CDC25 PHOSPHATASES; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME ACTIVATION; FLOW CYTOMETRY; HERPESVIRUS 4, HUMAN; HUMANS; LACTIC ACID; M PHASE CELL CYCLE CHECKPOINTS; NADPH OXIDASE; ONIUM COMPOUNDS; PROTO-ONCOGENE PROTEINS C-MYC; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRAL MATRIX PROTEINS;

EID: 84921647342     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.3726     Document Type: Article

References (42)

1. Vereide DT, Seto E, Chiu YF, Hayes M, Tagawa T, Grundhoff A, Hammerschmidt W and Sugden B: Epstein-Barr virus maintains lymphomas via its miRNAs. Oncogene 33:1258-1264, 2014.
2. Bornkamm GW: Epstein-Barr virus and the pathogenesis of Burkitt's lymphoma: more questions than answers. Int J Cancer 124:1745-1755, 2009.
3. Molyneux EM, Rochford R, Griffin B, Newton R, Jackson G, Menon G, Harrison CJ, Israels T and Bailey S: Burkitt's lymphoma. Lancet 379:1234-1244, 2012.
4. Drexler HG and Minowada J: History and classification of human leukemia-lymphoma cell lines. Leuk Lymphoma 31:305-316, 1998.
5. Bieging KT, Amick AC and Longnecker R: Epstein-Barr virus LMP2A bypasses p53 inactivation in a MYC model of lymphomagenesis. Proc Natl Acad Sci USA 106:17945-17950, 2009.
6. Lassoued S, Ben Ameur R, Ayadi W, Gargouri B, Ben Mansour R and Attia H: Epstein-Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines. Mol Cell Biochem 313:179-186, 2008.
7. Cerimele F, Battle T, Lynch R, Frank DA, Murad E, Cohen C, Macaron N, Sixbey J, Smith K, Watnick RS, Eliopoulos A, Shehata B and Arbiser JL: Reactive oxygen signaling and MAPK activation distinguish Epstein-Barr Virus (EBV)-positive versus EBV-negative Burkitt's lymphoma. Proc Natl Acad Sci USA 102:175-179, 2005.
8. Zheng H, Li LL, Hu DS, Deng XY and Cao Y: Role of Epstein-Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell Mol Immunol 4:185-196, 2007.
9. Ha YJ and Lee JR: Role of TNF receptor-associated factor 3 in the CD40 signaling by production of reactive oxygen species through association with p40phox, a cytosolic subunit of nicotinamide adenine dinucleotide phosphate oxidase. J Immunol 172:231-239, 2004.
10. Lambeth JD, Kawahara T and Diebold B: Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 43:319-331, 2007.
11. Devi GS, Prasad MH, Saraswathi I, Raghu D, Rao DN and Reddy PP: Free radicals antioxidant enzymes and lipid peroxidation in different types of leukemias. Clin Chim Acta 293:53-62, 2000.
12. Park SY, Chang I, Kim JY, Kang SW, Park SH, Singh K and Lee MS: Resistance of mitochondrial DNA-depleted cells against cell death: role of mitochondrial superoxide dismutase. J Biol Chem 279:7512-7520, 2004.
13. Behrend L, Henderson G and Zwacka RM: Reactive oxygen species in oncogenic transformation. Biochem Soc Trans 31:1441-1444, 2003.
14. Roth D, Krammer PH and Gulow K: Dynamin related protein 1-dependent mitochondrial fission regulates oxidative signalling in T cells. FEBS Lett 588:1749-1754, 2014.
15. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J and Huang P: Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell 10:241-252, 2006.
16. Lin B, Chen Z, Xu Y, Zhang H, Liu J and Qian X: 7-b, a novel amonafide analogue, cause growth inhibition and apoptosis in Raji cells via a ROS-mediated mitochondrial pathway. Leuk Res 35:646-656, 2011.
17. Fengling M, Fenju L, Wanxin W, Lijia Z, Jiandong T, Zu W, Xin Y and Qingxiang G: Rituximab sensitizes a Burkitt lymphoma cell line to cell killing by X-irradiation. Radiat Environ Biophys 48:371-378, 2009.
18. Kuang Y, Balakrishnan K, Gandhi V and Peng X: Hydrogen peroxide inducible DNA cross-linking agents: targeted anticancer prodrugs. J Am Chem Soc 133:19278-19281, 2011.
19. Fang J, Nakamura H and Iyer AK: Tumor-targeted induction of oxystress for cancer therapy. J Drug Target 15:475-486, 2007.
20. Hu ZY, Wang J, Cheng G, Zhu XF, Huang P, Yang D and Zeng YX: Apogossypolone targets mitochondria and light enhances its anticancer activity by stimulating generation of singlet oxygen and reactive oxygen species. Chin J Cancer 30:41-53, 2011.
21. Acharya A, Das I, Chandhok D and Saha T: Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxid Med Cell Longev 3:23-34, 2010.
22. Lee KW and Lee HJ: The roles of polyphenols in cancer chemoprevention. Biofactors 26:105-121, 2006.
23. Roy P, George J, Srivastava S, Tyagi S and Shukla Y: Inhibitory effects of tea polyphenols by targeting cyclooxygenase-2 through regulation of nuclear factor kappa B, Akt and p53 in rat mammary tumors. Invest New Drugs 29:225-231, 2011.
24. Talero E, Ávila-Roman J and Motilva V: Chemoprevention with phytonutrients and microalgae products in chronic inflammation and colon cancer. Curr Pharm Des 18:3939-3965, 2012.
25. Yamaura M, Mitsushita J, Furuta S, Kiniwa Y, Ashida A, Goto Y, Shang WH, Kubodera M, Kato M, Takata M, Saida T and Kamata T: NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res 69:2647-2654, 2009.
26. Bedard K and Krause KH: The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313, 2007.
27. Mbulaiteye SM, Anderson WF, Ferlay J, Bhatia K, Chang C, Rosenberg PS, Devesa SS and Parkin DM: Pediatric, elderly, and emerging adult-onset peaks in Burkitt's lymphoma incidence diagnosed in four continents, excluding Africa. Am J Hematol 87:573-578, 2012.
28. Gu JM, Lim SO, Oh SJ, Yoon SM, Seong JK and Jung G: HBx modulates iron regulatory protein 1-mediated iron metabolism via reactive oxygen species. Virus Res 133:167-177, 2008.
29. Silic-Benussi M, Cavallari I, Vajente N, Vidali S, Chieco-Bianchi L, Di Lisa F, Saggioro D, D'Agostino DM and Ciminale V: Redox regulation of T-cell turnover by the p13 protein of human T-cell leukemia virus type 1: distinct effects in primary versus transformed cells. Blood 116:54-62, 2010.
30. Hutzinger R, Feederle R, Mrazek J, Schiefermeier N, Balwierz PJ, Zavolan M, Polacek N, Delecluse HJ and Hüttenhofer A: Expression and processing of a small nucleolar RNA from the Epstein-Barr virus genome. PLoS Pathog 5:e1000547, 2009.
31. Lu W, Hu Y, Chen G, Chen Z, Zhang H, Wang F, Feng L, Pelicano H, Wang H, Keating MJ, Liu J, McKeehan W, Wang H, Luo Y and Huang P: Novel role of NOX in supporting aerobic glycolysis in cancer cells with mitochondrial dysfunction and as a potential target for cancer therapy. PLoS Biol 10:e1001326, 2012.
32. Prata C, Maraldi T, Fiorentini D, Zambonin L, Hakim G and Landi L: Nox-generated ROS modulate glucose uptake in a leukaemic cell line. Free Radic Res 42:405-414, 2008.
33. Han CY, Umemoto T, Omer M, Den Hartigh LJ, Chiba T, LeBoeuf R, Buller CL, Sweet IR, Pennathur S, Abel ED and Chait A: NADPH oxidase-derived reactive oxygen species increases expression of monocyte chemotactic factor genes in cultured adipocytes. J Biol Chem 287:10379-10393, 2012.
34. Block K and Gorin Y: Aiding and abetting roles of NOX oxidases in cellular transformation. Nat Rev Cancer 12:627-637, 2012.
35. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, Yamaura M, Ishizone S, Nakayama J, Konagai A, Hirose K, Kiyosawa K and Kamata T: Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signalregulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 25:3699-3707, 2006.
36. Singh MM, Irwin ME, Gao Y, Ban K, Shi P, Arlinghaus RB, Amin HM and Chandra J: Inhibition of the NADPH oxidase regulates heme oxygenase 1 expression in chronic myeloid leukemia. Cancer 118:3433-3445, 2012.
37. Ding Y, Chen ZJ, Liu S, Che D, Vetter M and Chang CH: Inhibition of Nox-4 activity by plumbagin, a plant-derived bioactive naphthoquinone. J Pharm Pharmacol 57:111-116, 2005.
38. Gianni D, Taulet N, Zhang H, der Mardirossian C, Kister J, Martinez L, Roush WR, Brown SJ, Bokoch GM and Rosen H: A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells. ACS Chem Biol 5:981-993, 2010.
39. Jaquet V, Marcoux J, Forest E, Leidal KG, McCormick S, Westermaier Y, Perozzo R, Plastre O, Fioraso-Cartier L, Diebold B, Scapozza L, Nauseef WM, Fieschi F, Krause KH and Bedard K: NADPH oxidase (NOX) isoforms are inhibited by celastrol with a dual mode of action. Br J Pharmacol 164:507-520, 2011.
40. Verbon EH, Post JA and Boonstra J: The influence of reactive oxygen species on cell cycle progression in mammalian cells. Gene 511:1-6, 2012.
41. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W, Keating MJ and 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 278:37832-37839, 2003.
42. Guo C, Pan ZG, Li DJ, Yun JP, Zheng MZ, Hu ZY, Cheng LZ and Zeng YX: The expression of p63 is associated with the differential stage in nasopharyngeal carcinoma and EBV infection. J Transl Med 4:23, 2006.