Combined incubation of colon carcinoma cells with phorbol ester and mitochondrial uncoupling agents results in synergic elevated reactive oxygen species levels and increased γ-glutamyltransferase expression

Molecular and Cellular Biochemistry

Volumn 388, Issue 1-2, 2014, Pages 149-156

  Pandur, Seila ^a   Ravuri, Chandra ^a   Moens, Ugo ^a   Huseby, Nils Erik ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Glutamyltransferase; Glutathione; Mitochondrial uncoupler; NADPH oxidase; Reactive oxygen species

Indexed keywords

ACETOPHENONES; BENZOPYRANS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL LINE, TUMOR; COLONIC NEOPLASMS; DRUG COMBINATIONS; DRUG SYNERGISM; ENZYME INHIBITORS; GAMMA-GLUTAMYLTRANSFERASE; HT29 CELLS; HUMANS; MITOCHONDRIA; NADPH OXIDASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TETRADECANOYLPHORBOL ACETATE; UNCOUPLING AGENTS;

EID: 84893861627     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1906-1     Document Type: Article

References (34)

1. Block K, Gorin Y (2012) Aiding and abetting roles of NOX oxidases in cellular transformation. Nat Rev Cancer 12:627-637. doi: 10.1038/nrc3339
2. Mitsushita J, Lambeth JD, Kamata T (2004) The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res 64:3580-3585. doi: 10.1158/0008-5472.CAN-03-3909 (Pubitemid 38657935)
3. Ralph SJ, Rodriguez-Enriquez S, Neuzil J, Saavedra E, Moreno-Sanchez R (2010) The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation - why mitochondria are targets for cancer therapy. Mol Aspects Med 31:145-170. doi: 10.1016/j.mam.2010.02.008
4. Daiber A (2010) Redox signaling (cross-talk) from and to mitochondria involves mitochondrial pores and reactive oxygen species. Biochim Biophys Acta 1797:897-906. doi: 10.1016/j.bbabio.2010.01.032
5. Kamata T (2009) Roles of Nox1 and other Nox isoforms in cancer development. Cancer Sci 100:1382-1388. doi: 10.1111/j.1349-7006.2009.01207.x
6. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181-189. doi: 10.1038/nri1312 (Pubitemid 38339084)
7. Aykin-Burns N, Ahmad IM, Zhu Y, Oberley LW, Spitz DR (2009) Increased levels of superoxide and H2O2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem J 418:29-37. doi: 10.1042/BJ20081258
8. Coso S, Harrison I, Harrison CB, Vinh A, Sobey CG, Drummond GR, Williams ED, Selemidis S (2012) NADPH oxidases as regulators of tumor angiogenesis: current and emerging concepts. Antioxid Redox Signal 16:1229-1247. doi: 10.1089/ars2011.4489
9. Kumar B, Koul S, Khandrika L, Meacham RB, Koul HK (2008) Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res 68:1777-1785. doi: 10.1158/0008-5472.CAN-07-5259 (Pubitemid 351416563)
10. Kajla S, Mondol AS, Nagasawa A, Zhang Y, Kato M, Matsuno K, Yabe-Nishimura C, Kamata T (2012) A crucial role for Nox 1 in redox-dependent regulation of Wnt-beta-catenin signaling. FASEB J 26:2049-2059. doi: 10.1096/fj.11-196360
11. Lu W, Hu Y, Chen G, Chen Z, Zhang H, Wang F, Feng L, Pelicano H, Wang H, Keating MJ, Liu J, McKeehan W, Luo Y, Huang P (2012) 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. doi: 10.1371/journal.pbio.1001326
12. Dikalov S (2011) Cross talk between mitochondria and NADPH oxidases. Free Radic Biol Med 51:1289-1301. doi: 10.1016/j.freeradbiomed.2011.06.033
13. Forman HJ, Zhang H, Rinna A (2009) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30:1-12. doi: 10.1016/j.mam.2008.08.006
14. Franco R, Cidlowski JA (2009) Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 16:1303-1314. doi: 10.1038/cdd.2009.107
15. Hanigan MH, Ricketts WA (1993) Extracellular glutathione is a source of cysteine for cells that express gamma-glutamyl transpeptidase. Biochemistry 32:6302-6306 (Pubitemid 23196889)
16. Obrador E, Carretero J, Ortega A, Medina I, Rodilla V, Pellicer JA, Estrela JM (2002) gamma-Glutamyl transpeptidase overexpression increases metastatic growth of B16 melanoma cells in the mouse liver. Hepatology 35:74-81. doi: 10.1053/jhep.2002.30277 (Pubitemid 34032545)
17. Ravuri C, Svineng G, Pankiv S, Huseby NE (2011) Endogenous production of reactive oxygen species by the NADPH oxidase complexes is a determinant of gamma-glutamyltransferase expression. Free Radic Res 45:600-610. doi: 10.3109/10715762.2011.564164
18. Ravuri C, Svineng G, Huseby NE (2013) Differential regulation of gamma-glutamyltransferase and glutamate cysteine ligase expression after mitochondrial uncoupling: gamma-glutamyltransferase is regulated in an Nrf2- and NFkappaB-independent manner. Free Radic Res 47:394-403. doi: 10.3109/10715762.2013.781270
19. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408. doi: 10.1006/meth2001.1262 (Pubitemid 34164012)
20. Ravuri C, Svineng G, Huseby NE (2013) Differential regulation of gamma-glutamyltransferase and glutamate cysteine ligase expression after mitochondrial uncoupling: gamma-glutamyltransferase is regulated in an Nrf2- and NFkappaB-independent manner. Free Radic Res. doi: 10.3109/10715762.2013.781270
21. Schulz E, Wenzel P, Munzel T, Daiber A (2012) Mitochondrial redox signaling: interaction of mitochondrial reactive oxygen species with other sources of oxidative stress. Antioxid Redox Signal. doi: 10.1089/ars.2012.4609
22. Wosniak J Jr, Santos CX, Kowaltowski AJ, Laurindo FR (2009) Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid Redox Signal 11:1265-1278. doi: 10.1089/ars.2009.2392
23. Desouki MM, Kulawiec M, Bansal S, Das GM, Singh KK (2005) Cross talk between mitochondria and superoxide generating NADPH oxidase in breast and ovarian tumors. Cancer Biol Ther 4:1367-1373 (Pubitemid 43131182)
24. Lee SB, Bae IH, Bae YS, Um HD (2006) Link between mitochondria and NADPH oxidase 1 isozyme for the sustained production of reactive oxygen species and cell death. J Biol Chem 281:36228-36235. doi: 10.1074/jbc.M606702200 (Pubitemid 46041357)
25. Rathore R, Zheng YM, Niu CF, Liu QH, Korde A, Ho YS, Wang YX (2008) Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2 +]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med 45:1223-1231. doi: 10.1016/j.freeradbiomed.2008.06. 012
26. Graham NA, Tahmasian M, Kohli B, Komisopoulou E, Zhu M, Vivanco I, Teitell MA, Wu H, Ribas A, Lo RS, Mellinghoff IK, Mischel PS, Graeber TG (2012) Glucose deprivation activates a metabolic and signaling amplification loop leading to cell death. Mol Syst Biol 8:589. doi: 10.1038/msb.2012.20
27. Nimnual AS, Taylor LJ, Bar-Sagi D (2003) Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5:236-241. doi: 10.1038/ncb938 (Pubitemid 36322251)
28. Hu Y, Lu W, Chen G, Wang P, Chen Z, Zhou Y, Ogasawara M, Trachootham D, Feng L, Pelicano H, Chiao PJ, Keating MJ, Garcia-Manero G, Huang P (2012) K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res 22:399-412. doi: 10.1038/cr.2011.145
29. Trachootham D, Alexandre J, Huang P (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8:579-591. doi: 10.1038/nrd2803
30. Huseby NE, Asare N, Wetting S, Mikkelsen IM, Mortensen B, Sveinbjornsson B, Wellman M (2003) Nitric oxide exposure of CC531 rat colon carcinoma cells induces gamma-glutamyltransferase which may counteract glutathione depletion and cell death. Free Radic Res 37:99-107 (Pubitemid 36124336)
31. Lieberman MW, Wiseman AL, Shi ZZ, Carter BZ, Barrios R, Ou CN, Chevez-Barrios P, Wang Y, Habib GM, Goodman JC, Huang SL, Lebovitz RM, Matzuk MM (1996) Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice. Proc Natl Acad Sci USA 93:7923-7926 (Pubitemid 26277140)
32. Reuter S, Schnekenburger M, Cristofanon S, Buck I, Teiten MH, Daubeuf S, Eifes S, Dicato M, Aggarwal BB, Visvikis A, Diederich M (2009) Tumor necrosis factor alpha induces gamma-glutamyltransferase expression via nuclear factor-kappaB in cooperation with Sp1. Biochem Pharmacol 77:397-411. doi: 10.1016/j.bcp.2008.09.041
33. West MB, Wickham S, Quinalty LM, Pavlovicz RE, Li C, Hanigan MH (2011) Autocatalytic cleavage of human gamma-glutamyl transpeptidase is highly dependent on N-glycosylation at asparagine 95. J Biol Chem 286:28876-28888. doi: 10.1074/jbc.M111.248823
34. Visvikis A, Pawlak A, Accaoui MJ, Ichino K, Leh H, Guellaen G, Wellman M (2001) Structure of the 5′ sequences of the human gamma- glutamyltransferase gene. Eur J Biochem 268:317-325 (Pubitemid 32862662)