UCP2 inhibition sensitizes breast cancer cells to therapeutic agents by increasing oxidative stress

Free Radical Biology and Medicine

Volumn 86, Issue , 2015, Pages 67-77

  Pons, Daniel Gabriel ^a,b   Nadal Serrano, Mercedes ^a,b   Torrens Mas, Margalida ^a,b   Valle, Adamo ^a,b   Oliver, Jordi ^a,b   Roca, Pilar ^a,b  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b Instituto de Salud Carlos III   (Spain)

Author keywords

Autophagic cell death; Cancer; Cisplatin; Oxidative stress; Resistance; ROS; Tamoxifen; UCP2

Indexed keywords

CISPLATIN; GENIPIN; REACTIVE OXYGEN METABOLITE; TAMOXIFEN; UNCOUPLING PROTEIN 2; ANTINEOPLASTIC AGENT; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2;

APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER CELL LINE; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; DRUG SENSITIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; OVERALL SURVIVAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; BREAST TUMOR; CELL SURVIVAL; DISEASE FREE SURVIVAL; DRUG RESISTANCE; FEMALE; GENE SILENCING; GENETICS; KAPLAN MEIER METHOD; MCF 7 CELL LINE; METABOLISM; MORTALITY;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CELL SURVIVAL; CISPLATIN; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; ION CHANNELS; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TAMOXIFEN;

EID: 84934764668     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.04.032     Document Type: Article

References (47)

1. G. Waris, and H. Ahsan Reactive oxygen species: role in the development of cancer and various chronic conditions J. Carcinog 5 2006 14
2. M. Nadal-Serrano, J. Sastre-Serra, D.G. Pons, A.M. Miro, J. Oliver, and P. Roca The ERalpha/ERbeta ratio determines oxidative stress in breast cancer cell lines in response to 17Beta-estradiol J. Cell Biochem. 113 2012 3178 3185
3. J. Sastre-Serra, M. Nadal-Serrano, D.G. Pons, A. Valle, I. Garau, M. Garcia-Bonafe, J. Oliver, and P. Roca The oxidative stress in breast tumors of postmenopausal women is ERalpha/ERbeta ratio dependent Free Radic. Biol. Med. 61C 2013 11 17
4. J. Sastre-Serra, A. Valle, M.M. Company, I. Garau, J. Oliver, and P. Roca Estrogen down-regulates uncoupling proteins and increases oxidative stress in breast cancer Free Radic. Biol. Med. 48 2010 506 512
5. S.P. Hussain, L.J. Hofseth, and C.C. Harris Radical causes of cancer Nat. Rev. Cancer 3 2003 276 285
6. R.M. Sainz, F. Lombo, and J.C. Mayo Radical decisions in cancer: redox control of cell growth and death Cancers(Basel) 4 2012 442 474
7. V. Nogueira, and N. Hay Molecular pathways: reactive oxygen species homeostasis in cancer cells and implications for cancer therapy Clin. Cancer Res. 19 2013 4309 4314
8. Y.H. Lee, B.S. Kang, and Y.S. Bae Premature senescence in human breast cancer and colon cancer cells by tamoxifen-mediated reactive oxygen species generation Life Sci. 97 2014 116 122
9. G. Baffy, Z. Derdak, and S.C. Robson Mitochondrial recoupling: a novel therapeutic strategy for cancer? Br. J. Cancer 105 2011 469 474
10. K.S. Mitochondrial Echtay uncoupling proteins - what is their physiological role? Free Radic. Biol. Med. 43 2007 1351 1371
11. A. Valle, J. Oliver, and P. Roca Role of uncoupling proteins in cancer Cancers(Basel) 2 2010 567 591
12. G. Baffy Uncoupling protein-2 and cancer Mitochondrion 10 2010 243 252
13. Z. Derdak, P. Fulop, E. Sabo, R. Tavares, E.P. Berthiaume, M.B. Resnick, G. Paragh, J.R. Wands, and G. Baffy Enhanced colon tumor induction in uncoupling protein-2 deficient mice is associated with NF-kappaB activation and oxidative stress Carcinogenesis 27 2006 956 961
14. Z. Derdak, N.M. Mark, G. Beldi, S.C. Robson, J.R. Wands, and G. Baffy The mitochondrial uncoupling protein-2 promotes chemoresistance in cancer cells Cancer Res. 68 2008 2813 2819
15. D. Robbins, and Y. Zhao New aspects of mitochondrial uncoupling proteins (UCPs) and their roles in tumorigenesis Int. J. Mol. Sci 12 2011 5285 5293
16. D.G. Pons, J. Sastre-Serra, M. Nadal-Serrano, A. Oliver, M. Garcia-Bonafe, I. Bover, P. Roca, and J. Oliver Initial activation status of the antioxidant response determines sensitivity to carboplatin/paclitaxel treatment of ovarian cancer Anticancer Res. 32 2012 4723 4728
17. V. Ayyasamy, K.M. Owens, M.M. Desouki, P. Liang, A. Bakin, K. Thangaraj, D.J. Buchsbaum, A.F. LoBuglio, and K.K. Singh Cellular model of Warburg effect identifies tumor promoting function of UCP2 in breast cancer and its suppression by genipin PLoS One 6 2011 e24792
18. A. Sayeed, Z. Meng, G. Luciani, L.C. Chen, J.L. Bennington, and S.H. Dairkee Negative regulation of UCP2 by TGFbeta signaling characterizes low and intermediate-grade primary breast cancer Cell Death Dis 1 2010 e53
19. E. Dalla Pozza, C. Fiorini, I. Dando, M. Menegazzi, A. Sgarbossa, C. Costanzo, M. Palmieri, and M. Donadelli Role of mitochondrial uncoupling protein 2 in cancer cell resistance to gemcitabine Biochim. Biophys. Acta 1823 2012 1856 1863
20. P.W. Ho, H.F. Liu, J.W. Ho, W.Y. Zhang, A.C. Chu, K.H. Kwok, X. Ge, K.H. Chan, D.B. Ramsden, and S.L. Ho Mitochondrial uncoupling protein-2 (UCP2) mediates leptin protection against MPP+ toxicity in neuronal cells Neurotox. Res. 17 2010 332 343
21. R.J. Mailloux, C.N. Adjeitey, and M.E. Harper Genipin-induced inhibition of uncoupling protein-2 sensitizes drug-resistant cancer cells to cytotoxic agents PLoS One 5 2010 e13289
22. T. Byrski, T. Huzarski, R. Dent, J. Gronwald, D. Zuziak, C. Cybulski, J. Kladny, B. Gorski, J. Lubinski, and S.A. Narod Response to neoadjuvant therapy with cisplatin in BRCA1-positive breast cancer patients Breast Cancer Res. Treat. 115 2009 359 363
23. L. Kelland The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 7 2007 573 584
24. C. Rivera-Guevara, and J. Camacho Tamoxifen and its new derivatives in cancer research Recent Pat. Anticancer Drug Discov 6 2011 237 245
25. P. Jordan, and M. Carmo-Fonseca Molecular mechanisms involved in cisplatin cytotoxicity Cell Mol. Life Sci. 57 2000 1229 1235
26. E.V. Jensen, and V.C. Jordan The estrogen receptor: a model for molecular medicine Clin. Cancer Res. 9 2003 1980 1989
27. R. Marullo, E. Werner, N. Degtyareva, B. Moore, G. Altavilla, S.S. Ramalingam, and P.W. Doetsch Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions PLoS One 8 2013 e81162
28. I. Dando, C. Fiorini, E.D. Pozza, C. Padroni, C. Costanzo, M. Palmieri, and M. Donadelli UCP2 inhibition triggers ROS-dependent nuclear translocation of GAPDH and autophagic cell death in pancreatic adenocarcinoma cells Biochim. Biophys. Acta 1833 2013 672 679
29. B. Gyorffy, A. Lanczky, A.C. Eklund, C. Denkert, J. Budczies, Q. Li, and Z. Szallasi An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients Breast Cancer Res. Treat. 123 2010 725 731
30. B. Gyorffy, P. Surowiak, J. Budczies, and A. Lanczky Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer PLoS One 8 2013 e82241
31. Q. Li, N.J. Birkbak, B. Gyorffy, Z. Szallasi, and A.C. Eklund Jetset: selecting the optimal microarray probe set to represent a gene BMC Bioinformatics 12 2011 474
32. D.G. Pons, M. Nadal-Serrano, M.M. Blanquer-Rossello, J. Sastre-Serra, J. Oliver, and P. Roca Genistein modulates proliferation and mitochondrial functionality in breast cancer cells depending on ERalpha/ERbeta ratio J. Cell Biochem. 115 2014 949 958
33. J.L. Martindale, and N.J. Holbrook Cellular response to oxidative stress: signaling for suicide and survival J. Cell Physiol. 192 2002 1 15
34. D. Trachootham, J. Alexandre, and P. Huang Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov. 8 2009 579 591
35. M.D. Brand, and T.C. Esteves Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3 Cell Metab. 2 2005 85 93
36. M. Nadal-Serrano, D.G. Pons, J. Sastre-Serra, M. Blanquer-Rossello Mdel, P. Roca, and J. Oliver Genistein modulates oxidative stress in breast cancer cell lines according to ERalpha/ERbeta ratio: effects on mitochondrial functionality, sirtuins, uncoupling protein 2 and antioxidant enzymes Int. J. Biochem. Cell Biol. 45 2013 2045 2051
37. P. Collins, C. Jones, S. Choudhury, L. Damelin, and H. Hodgson Increased expression of uncoupling protein 2 in HepG2 cells attenuates oxidative damage and apoptosis Liver Int. 25 2005 880 887
38. F.M. Santandreu, P. Roca, and J. Oliver Uncoupling protein-2 knockdown mediates the cytotoxic effects of cisplatin Free Radic. Biol. Med. 49 2010 658 666
39. H.W. Sung, W.H. Chang, C.Y. Ma, and M.H. Lee Crosslinking of biological tissues using genipin and/or carbodiimide J. Biomed. Mater. Res. A 64 2003 427 438
40. J.J. Hwang, H.N. Kim, J. Kim, D.H. Cho, M.J. Kim, Y.S. Kim, Y. Kim, S.J. Park, and J.Y. Koh Zinc(II) ion mediates tamoxifen-induced autophagy and cell death in MCF-7 breast cancer cell line Biometals 23 2010 997 1013
41. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18
42. K.L. Cook, A.N. Shajahan, and R. Clarke Autophagy and endocrine resistance in breast cancer Expert Rev. Anticancer Ther. 11 2011 1283 1294
43. U. Akar, A. Chaves-Reyez, M. Barria, A. Tari, A. Sanguino, Y. Kondo, S. Kondo, B. Arun, G. Lopez-Berestein, and B. Ozpolat Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells Autophagy 4 2008 669 679
44. W. Bursch, A. Ellinger, H. Kienzl, L. Torok, S. Pandey, M. Sikorska, R. Walker, and R.S. Hermann Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy Carcinogenesis 17 1996 1595 1607
45. J. Jakubowicz-Gil, R. Paduch, Z. Ulz, D. Badziul, K. Glowniak, and A. Gawron Cell death in HeLa cells upon imperatorin and cisplatin treatment Fol. Histochem. Cytobiol 50 2012 381 391
46. S. Mandlekar, and A.N. Kong Mechanisms of tamoxifen-induced apoptosis Apoptosis 6 2001 469 477
47. K. Seki, H. Yoshikawa, K. Shiiki, Y. Hamada, N. Akamatsu, and K. Tasaka Cisplatin (CDDP) specifically induces apoptosis via sequential activation of caspase-8, -3 and -6 in osteosarcoma Cancer Chemother. Pharmacol. 45 2000 199 206