Role of mitochondrial uncoupling protein 2 in cancer cell resistance to gemcitabine

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 10, 2012, Pages 1856-1863

  Dalla Pozza, Elisa ^a   Fiorini, Claudia ^a   Dando, Ilaria ^a   Menegazzi, Marta ^a   Sgarbossa, Anna ^a   Costanzo, Chiara ^a   Palmieri, Marta ^a   Donadelli, Massimo ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

Apoptosis; Cancer; Gemcitabine; Oxidative stress; Resistance; Uncoupling protein 2

Indexed keywords

ACETYLCYSTEINE; GEMCITABINE; GENIPIN; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; SUPEROXIDE; UNCOUPLING PROTEIN 2;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL GROWTH; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; FIBROBLAST; GENE SILENCING; HUMAN; HUMAN CELL; IC 50; MITOCHONDRION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ACETYLCYSTEINE; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ION CHANNELS; IRIDOIDS; MITOCHONDRIAL PROTEINS; NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES; RNA, MESSENGER; SUPEROXIDE DISMUTASE; SUPEROXIDES; UNCOUPLING AGENTS;

EID: 84864533886     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.06.007     Document Type: Article

References (36)

1. Donadelli M., Costanzo C., Beghelli S., Scupoli M.T., Dandrea M., Bonora A., Piacentini P., Budillon A., Caraglia M., Scarpa A., Palmieri M. Synergistic inhibition of pancreatic adenocarcinoma cell growth by trichostatin A and gemcitabine. Biochim. Biophys. Acta 2007, 1773:1095-1106.
2. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008, 7:11-20.
3. Kitano H. Cancer as a robust system: implications for anticancer therapy. Nat. Rev. Cancer 2004, 4:227-235.
4. Muller I., Niethammer D., Bruchelt G. Anthracycline-derived chemotherapeutics in apoptosis and free radical cytotoxicity (Review). Int. J. Mol. Med. 1998, 1:491-494.
5. Boss O., Muzzin P., Giacobino J.P. The uncoupling proteins, a review. Eur. J. Endocrinol. 1998, 139:1-9.
6. Fleury C., Sanchis D. The mitochondrial uncoupling protein-2: current status. Int. J. Biochem. Cell Biol. 1999, 31:1261-1278.
7. Baffy G. Uncoupling protein-2 and cancer. Mitochondrion 2010, 10:243-252.
8. Carretero M.V., Torres L., Latasa U., Garcia-Trevijano E.R., Prieto J., Mato J.M., Avila M.A. Transformed but not normal hepatocytes express UCP2. FEBS Lett. 1998, 439:55-58.
9. Horimoto M., Resnick M.B., Konkin T.A., Routhier J., Wands J.R., Baffy G. Expression of uncoupling protein-2 in human colon cancer. Clin. Cancer Res. 2004, 10:6203-6207.
10. Harper M.E., Antoniou A., Villalobos-Menuey E., Russo A., Trauger R., Vendemelio M., George A., Bartholomew R., Carlo D., Shaikh A., Kupperman J., Newell E.W., Bespalov I.A., Wallace S.S., Liu Y., Rogers J.R., Gibbs G.L., Leahy J.L., Camley R.E., Melamede R., Newell M.K. Characterization of a novel metabolic strategy used by drug-resistant tumor cells. FASEB J. 2002, 16:1550-1557.
11. Brand M.D., Affourtit C., Esteves T.C., Green K., Lambert A.J., Miwa S., Pakay J.L., Parker N. Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 2004, 37:755-767.
12. Brand M.D., Esteves T.C. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2005, 2:85-93.
13. Mattiasson G., Sullivan P.G. The emerging functions of UCP2 in health, disease, and therapeutics. Antioxid. Redox Signal. 2006, 8:1-38.
14. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
15. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
16. Derdak Z., Mark N.M., Beldi G., Robson S.C., Wands J.R., Baffy G. The mitochondrial uncoupling protein-2 promotes chemoresistance in cancer cells. Cancer Res. 2008, 68:2813-2819.
17. Mailloux R.J., Adjeitey C.N., Harper M.E. Genipin-induced inhibition of uncoupling protein-2 sensitizes drug-resistant cancer cells to cytotoxic agents. PLoS One 2010, 5:e13289.
18. Bruzzese F., Di Gennaro E., Avallone A., Pepe S., Arra C., Caraglia M., Tagliaferri P., Budillon A. Synergistic antitumor activity of epidermal growth factor receptor tyrosine kinase inhibitor gefitinib and IFN-alpha in head and neck cancer cells in vitro and in vivo. Clin. Cancer Res. 2006, 12:617-625.
19. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 1984, 22:27-55.
20. Kalyanaraman B., Darley-Usmar V., Davies K.J., Dennery P.A., Forman H.J., Grisham M.B., Mann G.E., Moore K., Roberts L.J., Ischiropoulos H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med. 2012, 52:1-6.
21. Robinson K.M., Janes M.S., Beckman J.S. The selective detection of mitochondrial superoxide by live cell imaging. Nat. Protoc. 2008, 3:941-947.
22. Robinson K.M., Janes M.S., Pehar M., Monette J.S., Ross M.F., Hagen T.M., Murphy M.P., Beckman J.S. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15038-15043.
23. Krauss S., Zhang C.Y., Lowell B.B. A significant portion of mitochondrial proton leak in intact thymocytes depends on expression of UCP2. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:118-122.
24. Rial E., Gonzalez-Barroso M., Fleury C., Iturrizaga S., Sanchis D., Jimenez-Jimenez J., Ricquier D., Goubern M., Bouillaud F. Retinoids activate proton transport by the uncoupling proteins UCP1 and UCP2. EMBO J. 1999, 18:5827-5833.
25. Zhang C.Y., Parton L.E., Ye C.P., Krauss S., Shen R., Lin C.T., Porco J.A., Lowell B.B. Genipin inhibits UCP2-mediated proton leak and acutely reverses obesity- and high glucose-induced beta cell dysfunction in isolated pancreatic islets. Cell Metab. 2006, 3:417-427.
26. Dalla Pozza E., Donadelli M., Costanzo C., Zaniboni T., Dando I., Franchini M., Arpicco S., Scarpa A., Palmieri M. Gemcitabine response in pancreatic adenocarcinoma cells is synergistically enhanced by dithiocarbamate derivatives. Free Radic. Biol. Med. 2011, 50:926-933.
27. Donadelli M., Dando I., Zaniboni T., Costanzo C., Dalla Pozza E., Scupoli M.T., Scarpa A., Zappavigna S., Marra M., Abbruzzese A., Bifulco M., Caraglia M., Palmieri M. Gemcitabine/cannabinoid combination triggers autophagy in pancreatic cancer cells through a ROS-mediated mechanism. Cell Death Dis. 2011, 2:e152.
28. Mini E., Nobili S., Caciagli B., Landini I., Mazzei T. Cellular pharmacology of gemcitabine. Ann. Oncol. 2006, 17(Suppl. 5):v7-v12.
29. Bergman A.M., Pinedo H.M., Peters G.J. Determinants of resistance to 2',2'-difluorodeoxycytidine (gemcitabine). Drug Resist. Updat. 2002, 5:19-33.
30. Hu G., Li F., Ouyang K., Xie F., Tang X., Wang K., Han S., Jiang Z., Zhu M., Wen D., Qin X., Zhang L. Intrinsic gemcitabine resistance in a novel pancreatic cancer cell line is associated with cancer stem cell-like phenotype. Int. J. Oncol. 2012, 40:798-806.
31. Oberkofler H., Klein K., Felder T.K., Krempler F., Patsch W. Role of peroxisome proliferator-activated receptor-gamma coactivator-1alpha in the transcriptional regulation of the human uncoupling protein 2 gene in INS-1E cells. Endocrinology 2006, 147:966-976.
32. Villarroya F., Iglesias R., Giralt M. PPARs in the control of uncoupling proteins gene expression. PPAR Res. 2007, 2007:74364.
33. Dumitru C.A., Sandalcioglu I.E., Wagner M., Weller M., Gulbins E. Lysosomal ceramide mediates gemcitabine-induced death of glioma cells. J. Mol. Med. 2009, 87:1123-1132.
34. Modrak D.E., Leon E., Goldenberg D.M., Gold D.V. Ceramide regulates gemcitabine-induced senescence and apoptosis in human pancreatic cancer cell lines. Mol. Cancer Res. 2009, 7:890-896.
35. Garcia-Ruiz C., Colell A., Mari M., Morales A., Fernandez-Checa J.C. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem. 1997, 272:11369-11377.
36. Laurent A., Nicco C., Chereau C., Goulvestre C., Alexandre J., Alves A., Levy E., Goldwasser F., Panis Y., Soubrane O., Weill B., Batteux F. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res. 2005, 65:948-956.