Synergism of arsenic trioxide and MG132 in Raji cells attained by targeting BNIP3, autophagy, and mitochondria with low doses of valproic acid and vincristine

European Journal of Cancer

Volumn 50, Issue 18, 2014, Pages 3243-3261

  Cavaliere, Victoria ^a   Lombardo, Tomás ^a   Costantino, Susana N ^a   Kornblihtt, Laura ^a   Alvarez, Elida M ^a   Blanco, Guillermo A ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Arsenic trioxide; Autophagy; BNIP3; Burkitt's lymphoma; MG132; Mitochondria; Mitophagy; Synergism; Targeted combined therapies; Valproic acid

Indexed keywords

ARSENIC TRIOXIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; PROTEIN BNIP3; VALPROIC ACID; VINCRISTINE; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; BNIP3 PROTEIN, HUMAN; ENZYME INHIBITOR; LEUPEPTIN; MEMBRANE PROTEIN; ONCOPROTEIN; ORGANOARSENIC DERIVATIVE; OXIDE;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DRUG ANTAGONISM; DRUG POTENTIATION; DRUG TARGETING; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL VOLUME; MITOPHAGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAJI CELL LINE; U937 CELL LINE; UPREGULATION; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; CELL SURVIVAL; DRUG EFFECTS; MEMBRANE POTENTIAL; METABOLISM; MITOCHONDRION; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ARSENICALS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; DRUG SYNERGISM; ENZYME INHIBITORS; HUMANS; LEUPEPTINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MITOCHONDRIA; OXIDES; PROTO-ONCOGENE PROTEINS; U937 CELLS; UP-REGULATION; VALPROIC ACID; VINCRISTINE;

EID: 84925226838     PISSN: 09598049     EISSN: 18790852     Source Type: Journal    
DOI: 10.1016/j.ejca.2014.09.012     Document Type: Article

References (58)

1. J. Hu, Y.F. Liu, C.F. Wu, F. Xu, Z.X. Shen, and Y.M. Zhu Long-term efficacy and safety of all-trans retinoic acid/arsenic trioxide-based therapy in newly diagnosed acute promyelocytic leukemia Proc Natl Acad Sci U S A 106 9 2009 3342 3347
2. L.C. Platanias Biological responses to arsenic compounds J Biol Chem 284 28 2009 18583 18587
3. A. Emadi, and S.D. Gore Arsenic trioxide - An old drug rediscovered Blood Rev 24 4-5 2010 191 199
4. L. Li, J. Wang, R.D. Ye, G. Shi, H. Jin, and X. Tang PML/RARalpha fusion protein mediates the unique sensitivity to arsenic cytotoxicity in acute promyelocytic leukemia cells: Mechanisms involve the impairment of cAMP signaling and the aberrant regulation of NADPH oxidase J Cell Physiol 217 2 2008 486 493
5. K. Ito, R. Bernardi, A. Morotti, S. Matsuoka, G. Saglio, and Y. Ikeda PML targeting eradicates quiescent leukaemia-initiating cells Nature 453 7198 2008 1072 1078
6. A.A. Chanan-Khan, I. Borrello, K.P. Lee, and D.E. Reece Development of target-specific treatments in multiple myeloma Br J Haematol 151 1 2010 3 15
7. T.C. Chou Drug combination studies and their synergy quantification using the Chou-Talalay method Cancer Res 70 2 2010 440 446
8. T. Lombardo, L. Anaya, L. Kornblihtt, and G. Blanco Median effect dose and combination index analysis of cytotoxic drugs using flow cytometry 2012 Intech Open Publisher Rijeka, Croatia
9. T. Lombardo, V. Cavaliere, S.N. Costantino, L. Kornblihtt, E.M. Alvarez, and G.A. Blanco Synergism between arsenite and proteasome inhibitor MG132 over cell death in myeloid leukaemic cells U937 and the induction of low levels of intracellular superoxide anion Toxicol Appl Pharmacol 258 3 2011 351 366
10. A.B. Al-Mehdi, V.M. Pastukh, B.M. Swiger, D.J. Reed, M.R. Patel, and G.C. Bardwell Perinuclear mitochondrial clustering creates an oxidant-rich nuclear domain required for hypoxia-induced transcription Sci Signal 5 231 2010 ra47
11. H.R. Mellor, and A.L. Harris The role of the hypoxia-inducible BH3-only proteins BNIP3 and BNIP3L in cancer Cancer Metastasis Rev 26 3-4 2007 553 566
12. R.A. Gottlieb, and A.B. Gustafsson Mitochondrial turnover in the heart Biochim Biophys Acta 1813 7 2011 1295 1301
13. R.A. Hanna, M.N. Quinsay, A.M. Orogo, K. Giang, S. Rikka, and A.B. Gustafsson Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy J Biol Chem 287 23 2012 19094 19104
14. T.R. Burton, and S.B. Gibson The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death Cell Death Differ 16 4 2009 515 523
15. L. Zhang, L. Li, H. Liu, K. Prabhakaran, X. Zhang, and J.L. Borowitz HIF-1alpha activation by a redox-sensitive pathway mediates cyanide-induced BNIP3 upregulation and mitochondrial-dependent cell death Free Radic Biol Med 43 1 2007 117 127
16. N.M. Mazure, and J. Pouyssegur Atypical BH3-domains of BNIP3 and BNIP3L lead to autophagy in hypoxia Autophagy 5 6 2009 868 869
17. J. Pouyssegur, F. Dayan, and N.M. Mazure Hypoxia signalling in cancer and approaches to enforce tumour regression Nature 441 7092 2006 437 443
18. K. Okatsu, K. Saisho, M. Shimanuki, K. Nakada, H. Shitara, and Y.S. Sou P62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria Genes Cells 15 8 2010 887 900
19. C. Vives-Bauza, C. Zhou, Y. Huang, M. Cui, R.L. de Vries, and J. Kim PINK1-dependent recruitment of Parkin to mitochondria in mitophagy Proc Natl Acad Sci U S A 107 1 2010 378 383
20. J.Y. Lee, Y. Nagano, J.P. Taylor, K.L. Lim, and T.P. Yao Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy J Cell Biol 189 4 2010 671 679
21. M.B. Azad, Y. Chen, E.S. Henson, J. Cizeau, E. McMillan-Ward, and S.J. Israels Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3 Autophagy 4 2 2008 195 204
22. N. Bristow, T.R. Burton, E.S. Henson, C. Ong-Justiniano, M. Brown, and S.B. Gibson Truncated forms of BNIP3 act as dominant negatives inhibiting hypoxia-induced cell death Biochim Biophys Acta 1812 3 2011 302 311
23. T. Kanzawa, L. Zhang, L. Xiao, I.M. Germano, Y. Kondo, and S. Kondo Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3 Oncogene 24 6 2005 980 991
24. M. Murai, M. Toyota, A. Satoh, H. Suzuki, K. Akino, and H. Mita Aberrant DNA methylation associated with silencing BNIP3 gene expression in haematopoietic tumours Br J Cancer 92 6 2005 1165 1172
25. V. Cavaliere, D.L. Papademetrio, T. Lombardo, S.N. Costantino, G.A. Blanco, and E.M. Alvarez Caffeic acid phenylethyl ester and MG132, two novel nonconventional chemotherapeutic agents, induce apoptosis of human leukemic cells by disrupting mitochondrial function Target Oncol 2013
26. V. Cavaliere, D.L. Papademetrio, E.M. Alvarez, and G.A. Blanco Haemostatic and immune role of cellular clotting in the sipunculan Themiste petricola Cell Tissue Res 339 3 2010 597 611
27. R.I. Cordo Russo, M.G. Garcia, L. Alaniz, G. Blanco, E. Alvarez, and S.E. Hajos Hyaluronan oligosaccharides sensitize lymphoma resistant cell lines to vincristine by modulating P-glycoprotein activity and PI3K/Akt pathway Int J Cancer 122 5 2008 1012 1018
28. G.L. Semenza Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning Biochim Biophys Acta 1813 7 2011 1263 1268
29. D.B. Munafo, and M.I. Colombo A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation J Cell Sci 114 Pt 20 2001 3619 3629
30. D.H. Lee, and A.L. Goldberg Proteasome inhibitors: valuable new tools for cell biologists Trends Cell Biol 8 10 1998 397 403
31. A. Kloss, S. Meiners, A. Ludwig, and B. Dahlmann Multiple cardiac proteasome subtypes differ in their susceptibility to proteasome inhibitors Cardiovasc Res 85 2 2013 367 375
32. Y.H. Han, H.J. Moon, B.R. You, and W.H. Park The effect of MG132, a proteasome inhibitor on HeLa cells in relation to cell growth, reactive oxygen species and GSH Oncol Rep 22 1 2009 215 221
33. R. Oerlemans, N.E. Franke, Y.G. Assaraf, J. Cloos, I. van Zantwijk, and C.R. Berkers Molecular basis of bortezomib resistance: proteasome subunit beta5 (PSMB5) gene mutation and overexpression of PSMB5 protein Blood 112 6 2008 2489 2499
34. S. Kumar, and S.V. Rajkumar Many facets of bortezomib resistance/susceptibility Blood 112 6 2008 2177 2178
35. W.X. Ding, H.M. Ni, W. Gao, T. Yoshimori, D.B. Stolz, and D. Ron Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability Am J Pathol 171 2 2007 513 524
36. D.J. Goussetis, J.K. Altman, H. Glaser, J.L. McNeer, M.S. Tallman, and L.C. Platanias Autophagy is a critical mechanism for the induction of the antileukemic effects of arsenic trioxide J Biol Chem 285 39 2010 29989 29997
37. P. Isakson, M. Bjoras, S.O. Boe, and A. Simonsen Autophagy contributes to therapy-induced degradation of the PML/RARA oncoprotein Blood 116 13 2010 2324 2331
38. A. Giatromanolaki, M.I. Koukourakis, K.C. Gatter, A.L. Harris, and E. Sivridis BNIP3 expression in endometrial cancer relates to active hypoxia inducible factor 1alpha pathway and prognosis J Clin Pathol 61 2 2008 217 220
39. H.M. Sowter, M. Ferguson, C. Pym, P. Watson, S.B. Fox, and C. Han Expression of the cell death genes BNip3 and NIX in ductal carcinoma in situ of the breast; correlation of BNip3 levels with necrosis and grade J Pathol 201 4 2003 573 580
40. C. Leo, L.C. Horn, and M. Hockel Hypoxia and expression of the proapoptotic regulator BNIP3 in cervical cancer Int J Gynecol Cancer 16 3 2006 1314 1320
41. J. Okami, D.M. Simeone, and C.D. Logsdon Silencing of the hypoxia-inducible cell death protein BNIP3 in pancreatic cancer Cancer Res 64 15 2004 5338 5346
42. M. Erkan, J. Kleeff, I. Esposito, T. Giese, K. Ketterer, and M.W. Buchler Loss of BNIP3 expression is a late event in pancreatic cancer contributing to chemoresistance and worsened prognosis Oncogene 24 27 2005 4421 4432
43. M. Murai, M. Toyota, H. Suzuki, A. Satoh, Y. Sasaki, and K. Akino Aberrant methylation and silencing of the BNIP3 gene in colorectal and gastric cancer Clin Cancer Res 11 3 2005 1021 1027
44. G. Heller, W.M. Schmidt, B. Ziegler, S. Holzer, L. Mullauer, and M. Bilban Genome-wide transcriptional response to 5-aza-2′-deoxycytidine and trichostatin a in multiple myeloma cells Cancer Res 68 1 2008 44 54
45. M. Ishida, M. Sunamura, T. Furukawa, M. Akada, H. Fujimura, and E. Shibuya Elucidation of the relationship of BNIP3 expression to gemcitabine chemosensitivity and prognosis World J Gastroenterol 13 34 2007 4593 4597
46. A. Hamacher-Brady, N.R. Brady, S.E. Logue, M.R. Sayen, M. Jinno, and L.A. Kirshenbaum Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy Cell Death Differ 14 1 2007 146 157
47. G. Bellot, R. Garcia-Medina, P. Gounon, J. Chiche, D. Roux, and J. Pouyssegur Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains Mol Cell Biol 29 10 2009 2570 2581
48. T.R. Burton, E.S. Henson, P. Baijal, D.D. Eisenstat, and S.B. Gibson The pro-cell death Bcl-2 family member, BNIP3, is localized to the nucleus of human glial cells: Implications for glioblastoma multiforme tumor cell survival under hypoxia Int J Cancer 118 7 2006 1660 1669
49. K.M. Regula, K. Ens, and L.A. Kirshenbaum Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes Circ Res 91 3 2002 226 231
50. C. Vande Velde, J. Cizeau, D. Dubik, J. Alimonti, T. Brown, and S. Israels BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore Mol Cell Biol 20 15 2000 5454 5468
51. D.A. Kubli, J.E. Ycaza, and A.B. Gustafsson Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak Biochem J 405 3 2007 407 415
52. G. Twig, A. Elorza, A.J. Molina, H. Mohamed, J.D. Wikstrom, and G. Walzer Fission and selective fusion govern mitochondrial segregation and elimination by autophagy Embo J 27 2 2008 433 446
53. W.X. Ding, and X.M. Yin Mitophagy: mechanisms, pathophysiological roles, and analysis Biol Chem 393 7 2012 547 564
54. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, and K. Adeli Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 4 2012 445 544
55. M.N. Quinsay, R.L. Thomas, Y. Lee, and A.B. Gustafsson Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore Autophagy 6 7 2010 855 862
56. S. Rikka, M.N. Quinsay, R.L. Thomas, D.A. Kubli, X. Zhang, and A.N. Murphy Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover Cell Death Differ 18 4 2011 721 731
57. G. García-Manero Therapeutic modalities and new molecular targets in MDS 2011 Springer London, UK
58. L. Jia, G. Gopinathan, J.T. Sukumar, and J.G. Gribben Blocking autophagy prevents bortezomib-induced NF-kappaB activation by reducing I-kappaBalpha degradation in lymphoma cells PLoS One 7 2 2012 e32584