Doxorubicin induces apoptosis in Jurkat cells by mitochondria-dependent and mitochondria-independent mechanisms under normoxic and hypoxic conditions

Anti-Cancer Drugs

Volumn 26, Issue 6, 2015, Pages 583-598

  Mendivil Perez, Miguel ^a   Velez Pardo, Carlos ^a   Jimenez Del Rio, Marlene ^a  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

apoptosis; apoptosis inducing factor; caspase 3; DJ 1; doxorubicin; HIF 1 ; NF B; oxidative stress; p53; Parkin; PINK 1

Indexed keywords

APOPTOSIS INDUCING FACTOR; CASPASE 3; DOXORUBICIN; HYDROGEN PEROXIDE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARKIN; PROTEIN C JUN; PROTEIN P53; ACETYLCYSTEINE; AIFM1 PROTEIN, HUMAN; ANTINEOPLASTIC ANTIBIOTIC; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ONCOPROTEIN; PARK7 PROTEIN, HUMAN; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; SIGNAL PEPTIDE; UBIQUITIN PROTEIN LIGASE;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL DEATH; COMPARATIVE STUDY; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG CYTOTOXICITY; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYPOXIA; IMAGE ANALYSIS; IMMUNOFLUORESCENCE TEST; JURKAT CELL LINE; MICROPHOTOGRAPHY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NORMOXIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL HYPOXIA; DRUG EFFECTS; METABOLISM;

ACETYLCYSTEINE; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CASPASE 3; CELL HYPOXIA; DOXORUBICIN; HUMANS; HYDROGEN PEROXIDE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JURKAT CELLS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NF-KAPPA B; ONCOGENE PROTEINS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-JUN; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES;

EID: 84930660341     PISSN: 09594973     EISSN: 14735741     Source Type: Journal    
DOI: 10.1097/CAD.0000000000000223     Document Type: Article

References (58)

1. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al. SEER cancer statistics review, 1975-2010. 2013; Bethesda, MD: National Cancer Institute. Available at: http://seer.cancer.gov/csr/1975-2010/.
2. Kantarjian H, Thomas D, O'Brien S, Cortes J, Giles F, Jeha S, et al. Long-term follow-up results of hyperfractionated cyclophosphamide, vincristine, doxorubicin, and dexamethasone (Hyper-CVAD), a dose-intensive regimen, in adult acute lymphocytic leukemia. Cancer 2004; 101:2788-2801.
3. Lowas SR, Marks D, Malempati S. Prevalence of transient hyperglycemia during induction chemotherapy for pediatric acute lymphoblastic leukemia. Pediatr Blood Cancer 2009; 52:814-818.
4. Weng AP, Ferrando AA, Lee W, Morris JP, Silverman LB, Sanchez-Irizarry C, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004; 306:269-271.
5. Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat 2011; 14:191-201.
6. Frolova O, Samudio I, Benito JM, Jacamo R, Kornblau SM, Markovic A, et al. Regulation of HIF-1a signaling and chemoresistance in acute lymphocytic leukemia under hypoxic conditions of the bone marrow microenvironment. Cancer Biol Ther 2012; 13:858-870.
7. Cui XY, Skretting G, Jing Y, Sun H, Sandset PM, Sun L. Hypoxia influences stem cell-like properties in multidrug resistant K562 leukemic cells. Blood Cells Mol Dis 2013; 51:177-184.
8. Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm 2011; 8:1996-2011.
9. Breier A, Gibalova L, Seres M, Barancik M, Sulova Z. New insight into p-glycoprotein as a drug target. Anticancer Agents Med Chem 2013; 13:159-170.
10. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-674.
11. Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011; 147:742-758.
12. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009; 16:3-11.
13. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19:107-120.
14. Gewirtz DA. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 1999; 57:727-741.
15. Denard B, Lee C, Ye J. Doxorubicin blocks proliferation of cancer cells through proteolytic activation of CREB3L1. Elife (Cambridge) 2012; 1: e00090.
16. Mizutani H, Tada-Oikawa S, Hiraku Y, Kojima M, Kawanishi S. Mechanism of apoptosis induced by doxorubicin through the generation of hydrogen peroxide. Life Sci 2005; 76:1439-1453.
17. Gamen S, Anel A, Pérez-Galán P, Lasierra P, Johnson D, Piñeiro A, et al. Doxorubicin treatment activates a Z-VAD-sensitive caspase, which causes deltapsim loss, caspase-9 activity, and apoptosis in Jurkat cells. Exp Cell Res 2000; 258:223-235.
18. Brantley-Finley C, Lyle CS, Du L, Goodwin ME, Hall T, Szwedo D, et al. The JNK, ERK and p53 pathways play distinct roles in apoptosis mediated by the antitumor agents vinblastine, doxorubicin, and etoposide. Biochem Pharmacol 2003; 66:459-469.
19. van Delft MF, Smith DP, Lahoud MH, Huang DC, Adams JM. Apoptosis and non-inflammatory phagocytosis can be induced by mitochondrial damage without caspases. Cell Death Differ 2010; 17:821-832.
20. López-Royuela N, Pérez-Galán P, Galán-Malo P, Yuste VJ, Anel A, Susín SA, et al. Different contribution of BH3-only proteins and caspases to doxorubicin-induced apoptosis in p53-deficient leukemia cells. Biochem Pharmacol 2010; 79:1746-5178.
21. Tsang WP, Chau SP, Kong SK, Fung KP, Kwok TT. Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci 2003; 73:2047-2058.
22. Aguiló JI, Iturralde M, Monleón I, Iñarrea P, Pardo J, Martínez-Lorenzo MJ, et al. Cytotoxicity of quinone drugs on highly proliferative human leukemia T cells: reactive oxygen species generation and inactive shortened SOD1 isoform implications. Chem Biol Interact 2012; 198:18-28.
23. Ashikawa K, Shishodia S, Fokt I, Priebe W, Aggarwal BB. Evidence that activation of nuclear factor-kappaB is essential for the cytotoxic effects of doxorubicin and its analogues. Biochem Pharmacol 2004; 67:353-364.
24. Campbell KJ, Rocha S, Perkins ND. Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol Cell 2004; 13:853-865.
25. Ho WC, Dickson KM, Barker PA. Nuclear factor-kappaB induced by doxorubicin is deficient in phosphorylation and acetylation and represses nuclear factor-kappaB-dependent transcription in cancer cells. Cancer Res 2005; 65:4273-4281.
26. Bednarski BK, Baldwin AS, Kim HJ. Addressing reported pro-apoptotic functions of NF-kappaB: targeted inhibition of canonical NF-kappaB enhances the apoptotic effects of doxorubicin. PLoS One 2009; 4:e6992.
27. Tacar O, Sriamornsak P, Dass CR. Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol 2013; 65:157-170.
28. Mendivil-Perez M, Velez-Pardo C, Jimenez-Del-Rio M. TPEN induces apoptosis independently of zinc chelator activity in a model of acute lymphoblastic leukemia and ex vivo acute leukemia cells through oxidative stress and mitochondria caspase-3-and AIF-dependent pathways. Oxid Med Cell Longev 2012; 2012:313275.
29. Mendivil-Perez M, Jimenez-Del-Rio M, Velez-Pardo C. Response to rotenone is glucose-sensitive in a model of human acute lymphoblastic leukemia: involvement of oxidative stress mechanism, DJ-1, Parkin, and PINK-1 proteins. Oxid Med Cell Longev 2014; 2014:457154.
30. Mendivil-Perez M, Jimenez-Del-Rio M, Velez-Pardo C. Glucose starvation induces apoptosis in a model of acute T leukemia dependent on caspase-3 and apoptosis-inducing factor: a therapeutic strategy. Nutr Cancer 2013; 65:99-109.
31. Jimenez-Del-Rio M, Velez-Pardo C. The bad, the good, and the ugly about oxidative stress. Oxid Med Cell Longev 2012; 2012:163913.
32. Winklhofer KF. Parkin and mitochondrial quality control: toward assembling the puzzle. Trends Cell Biol 2014; 24:332-341.
33. Yang YX, Muqit MM, Latchman DS. Induction of parkin expression in the presence of oxidative stress. Eur J Neurosci 2006; 24:1366-1372.
34. Wilson MA. The role of cysteine oxidation in DJ-1 function and dysfunction. Antioxid Redox Signal 2011; 15:111-122.
35. Cookson MR. Parkinsonism due to mutations in PINK1, parkin, and DJ-1 and oxidative stress and mitochondrial pathways. Cold Spring Harb Perspect Med 2012; 2:a009415.
36. Liu H, Wang M, Li M, Wang D, Rao Q, Wang Y, et al. Expression and role of DJ-1 in leukemia. Biochem Biophys Res Commun 2008; 375:477-483.
37. Agirre X, Román-Gómez J, Vázquez I, Jiménez-Velasco A, Garate L, Montiel-Duarte C, et al. Abnormal methylation of the common PARK2 and PACRG promoter is associated with downregulation of gene expression in acute lymphoblastic leukemia and chronic myeloid leukemia. Int J Cancer 2006; 118:1945-1953.
38. Zhang C, Lin M,Wu R,Wang X, Yang B, Levine AJ, et al. Parkin, a p53 target gene, mediates the role of p53 in glucose metabolism and the Warburg effect. Proc Natl Acad Sci USA 2011; 108:16259-16264.
39. Henn IH, Bouman L, Schlehe JS, Schlierf A, Schramm JE, Wegener E, et al. Parkin mediates neuroprotection through activation of IkappaB kinase/ nuclear factor-kappaB signaling. J Neurosci 2007; 27:1868-1878.
40. Sha D, Chin LS, Li L. Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum Mol Genet 2010; 19:352-363.
41. Fiegl M, Samudio I, Clise-Dwyer K, Burks JK, Mnjoyan Z, Andreeff M. CXCR4 expression and biologic activity in acute myeloid leukemia are dependent on oxygen partial pressure. Blood 2009; 113:1504-1512.
42. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006; 70:1469-1480.
43. Wu D, Yotnda P. Induction and testing of hypoxia in cell culture. J Vis Exp 2011; 12:pii-2899.
44. Marinho HS, Real C, Cyrne L, Soares H, Antunes F. Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol 2014; 2:535-562.
45. Leite M, Quinta-Costa M, Leite PS, Guimarães JE. Critical evaluation of techniques to detect and measure cell death-study in a model of UV radiation of the leukaemic cell line HL60. Anal Cell Pathol 1999; 19:139-151.
46. Mikami T, Koyama T, Imakiire A, Yamamoto K, Furuhata M, Toyota H, et al. Cjun N-terminal kinase activation is required for apoptotic cell death induced by TNF-related apoptosis-inducing ligand plus DNA-damaging agents in sarcoma cell lines. Anticancer Res 2006; 26:1153-1160.
47. Inanami O, Takahashi K, Yoshito A, Kuwabara M. Hydrogen peroxide-induced activation of SAPK/JNK regulated by phosphatidylinositol 3-kinase in Chinese hamster V79 cells. Antioxid Redox Signal 1999; 1:113-121.
48. Kamata H, Manabe T, Oka S, Kamata K, Hirata H. Hydrogen peroxide activates IkappaB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 2002; 519:231-237.
49. Takada Y, Mukhopadhyay A, Kundu GC, Mahabeleshwar GH, Singh S, Aggarwal BB. Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk proteintyrosine kinase. J Biol Chem 2003; 278:24233-24241.
50. Yang F, Chen H, Liu Y, Yin K, Wang Y, Li X, et al. Doxorubicin caused apoptosis of mesenchymal stem cells via p38, JNK and p53 pathway. Cell Physiol Biochem 2013; 32:1072-1082.
51. McNeill-Blue C, Wetmore BA, Sanchez JF, Freed WJ, Merrick BA. Apoptosis mediated by p53 in rat neural AF5 cells following treatment with hydrogen peroxide and staurosporine. Brain Res 2006; 1112:1-15.
52. Hangen E, Blomgren K, Bénit P, Kroemer G, Modjtahedi N. Life with or without AIF. Trends Biochem Sci 2010; 35:278-287.
53. Greene AW, Grenier K, Aguileta MA, Muise S, Farazifard R, Haque ME, et al. Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment. EMBO Rep 2012; 13:378-385.
54. Okatsu K, Oka T, Iguchi M, Imamura K, Kosako H, Tani N, et al. PINK1 autophosphorylation upon membrane potential dissipation is essential for Parkin recruitment to damaged mitochondria. Nat Commun 2012; 3:1016.
55. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, et al. PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2012; 2:120080.
56. Chan NC, Chan DC. Parkin uses the UPS to ship off dysfunctional mitochondria. Autophagy 2011; 7:771-772.
57. Benito J, Shi Y, Szymanska B, Carol H, Boehm I, Lu H, et al. Pronounced hypoxia in models of murine and human leukemia: high efficacy of hypoxiaactivated prodrug PR-104. PLoS One 2011; 6:e23108.
58. Rohwer N, Dame C, Haugstetter A, Wiedenmann B, Detjen K, Schmitt CA, et al. Hypoxia-inducible factor 1alpha determines gastric cancer chemosensitivity via modulation of p53 and NF-kappaB. PLoS One 2010; 5: e12038.