Inhibition of mTOR-dependent autophagy sensitizes leukemic cells to cytarabine-induced apoptotic death

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Bosnjak, Mihajlo ^a   Ristic, Biljana ^a   Arsikin, Katarina ^a   Mircic, Aleksandar ^a   Suzin Zivkovic, Violeta ^a   Perovic, Vladimir ^a   Bogdanovic, Andrija ^a   Paunovic, Verica ^a   Markovic, Ivanka ^a   Bumbasirevic, Vladimir ^a   Trajkovic, Vladimir ^a   Harhaji Trajkovic, Ljubica ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY PROTEIN 5; BAFILOMYCIN A1; CHLOROQUINE; CYTARABINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEUCINE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN P62; S6 KINASE; ANTINEOPLASTIC ANTIMETABOLITE; P62 PROTEIN, HUMAN; RNA BINDING PROTEIN; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; ATG4 GENE; ATG5 GENE; ATG7 GENE; AUTOPHAGOSOME; AUTOPHAGY; CELL PROTECTION; CELL VACUOLE; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LEUKEMIA CELL; LEUKEMIA CELL LINE; LEUKOCYTE; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN DEGRADATION; RNA INTERFERENCE; TRANSMISSION ELECTRON MICROSCOPY; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LEUKEMIA; METABOLISM; MONONUCLEAR CELL; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CYTARABINE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; LEUKEMIA; LEUKOCYTES, MONONUCLEAR; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84899414494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094374     Document Type: Article

References (53)

1. Lamba JK (2009) Genetic factors influencing cytarabine therapy. Pharmacogenomics 10: 1657-1674.
2. Novotny L, Rauko P (2009) Cytarabine conjugates with biologically active molecules and their potential anticancer activity. Neoplasma 56: 177-186.
3. Stentoft J (1990) The toxicity of cytarabine. Drug Saf 5: 7-27.
4. Yang Z, Klionsky DJ (2010) Mammalian autophagy: core molecular machinery and signaling regulation. Curr Opin Cell Biol 22: 124-131.
5. Puissant A, Robert G, Auberger P (2010) Targeting autophagy to fight hematopoietic malignancies. Cell Cycle 9: 3470-3478.
6. Cheng J, Wei HL, Chen J, Xie B (2012) Antitumor effect of arsenic trioxide in human K562 and K562/ADM cells by autophagy. Toxicol Mech Methods 22: 512-519.
7. Grander D, Kharaziha P, Laane E, Pokrovskaja K, Panaretakis T (2009) Autophagy as the main means of cytotoxicity by glucocorticoids in hematological malignancies. Autophagy 5: 1198-1200.
8. Schnekenburger M, Grandjenette C, Ghelfi J, Karius T, Foliguet B, et al. (2011) Sustained exposure to the DNA demethylating agent, 29 -deoxy-5-azacytidine, leads to apoptotic cell death in chronic myeloid leukemia by promoting differentiation, senescence, and autophagy. Biochem Pharmacol 81: 364-378.
9. Robert G, Ben Sahra I, Puissant A, Colosetti P, Belhacene N, et al. (2009) Acadesine kills chronic myelogenous leukemia (CML) cells through PKC-dependent induction of autophagic cell death. PLoS One 4: e7889.
10. Puissant A, Robert G, Fenouille N, Luciano F, Cassuto JP, et al. (2010) Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation. Cancer Res 70: 1042-1052.
11. Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, et al. (2009) Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest 119: 1109-1123.
12. Han W, Sun J, Feng L, Wang K, Li D, et al. (2011) Autophagy inhibition enhances daunorubicin-induced apoptosis in K562 cells. PLoS One 6: e28491.
13. Mahoney E, Lucas DM, Gupta SV, Wagner AJ, Herman SE, et al. (2012) ER stress and autophagy: new discoveries in the mechanism of action and drug resistance of the cyclin-dependent kinase inhibitor flavopiridol. Blood 120: 1262-1273.
14. Evangelisti C, Ricci F, Tazzari P, Chiarini F, Battistelli M, et al. (2011) Preclinical testing of the Akt inhibitor triciribine in T-cell acute lymphoblastic leukemia. J Cell Physiol 226: 822-831.
15. Calabretta B, Salomoni P (2011) Inhibition of autophagy: a new strategy to enhance sensitivity of chronic myeloid leukemia stem cells to tyrosine kinase inhibitors. Leuk Lymphoma 52 Suppl 1: 54-59.
16. Wang J, Whiteman MW, Lian H, Wang G, Singh A, et al. (2009) A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J Biol Chem 284: 21412-21424.
17. Jain MV, Paczulla AM, Klonisch T, Dimgba FN, Rao SB, et al. (2013) Interconnections between apoptotic, autophagic and necrotic pathways: implications for cancer therapy development. J Cell Mol Med 17: 12-29.
18. Fimia GM, Piacentini M (2010) Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol Life Sci 67: 1581-1588.
19. Notte A, Leclere L, Michiels C (2011) Autophagy as a mediator of chemotherapy-induced cell death in cancer. Biochem Pharmacol 82: 427-434.
20. Banerji V, Gibson SB (2012) Targeting metabolism and autophagy in the context of haematologic malignancies. Int J Cell Biol 2012: 595976.
21. Ishdorj G, Li L, Gibson SB (2012) Regulation of autophagy in hematological malignancies: role of reactive oxygen species. Leuk Lymphoma 53: 26-33.
22. Liu L, Yang M, Kang R, Wang Z, Zhao Y, et al. (2011) HMGB1-induced autophagy promotes chemotherapy resistance in leukemia cells. Leukemia 25: 23-31.
23. Ohtomo T, Miyazawa K, Naito M, Moriya S, Kuroda M, et al. (2010) Cytoprotective effect of imatinib mesylate in non-BCR-ABL-expressing cells along with autophagosome formation. Biochem Biophys Res Commun 391: 310-315.
24. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, et al. (2009) The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood 114: 937-951.
25. Connolly DT, Knight MB, Harakas NK, Wittwer AJ, Feder J (1986) Determination of the number of endothelial cells in culture using an acid phosphatase assay. Anal Biochem 152: 136-140. (Pubitemid 16140445)
26. Kaludjerovic GN, Miljkovic D, Momcilovic M, Djinovic VM, Mostarica Stojkovic M, et al. (2005) Novel platinum(IV) complexes induce rapid tumor cell death in vitro. Int J Cancer 116: 479-486. (Pubitemid 40993347)
27. Sadowski-Debbing K, Coy JF, Mier W, Hug H, Los M (2002) Caspases-their role in apoptosis and other physiological processes as revealed by knock-out studies. Arch Immunol Ther Exp (Warsz) 50: 19-34.
28. Schulze-Osthoff K, Ferrari D, Los M, Wesselborg S, Peter ME (1998) Apoptosis signaling by death receptors. Eur J Biochem 254: 439-459. (Pubitemid 28308094)
29. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, et al. (2008) Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 283: 22847-22857.
30. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, et al. (2009) In search of an "autophagomometer". Autophagy 5: 585-589.
31. Kimball SR, Shantz LM, Horetsky RL, Jefferson LS (1999) Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J Biol Chem 274: 11647-11652.
32. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140: 313-326.
33. Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelarova H, Meijer AJ (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246. (Pubitemid 27060408)
34. Alers S, Loffler AS, Wesselborg S, Stork B (2012) Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 32: 2-11.
35. Jung CH, Ro SH, Cao J, Otto NM, Kim DH (2010) mTOR regulation of autophagy. FEBS Lett 584: 1287-1295.
36. Huang Y, Hou JK, Chen TT, Zhao XY, Yan ZW, et al. (2011) PML-RARalpha enhances constitutive autophagic activity through inhibiting the Akt/mTOR pathway. Autophagy 7: 1132-1144.
37. Li J, Liu R, Lei Y, Wang K, Lau QC, et al. (2010) Proteomic analysis revealed association of aberrant ROS signaling with suberoylanilide hydroxamic acid-induced autophagy in Jurkat T-leukemia cells. Autophagy 6: 711-724.
38. Grimaldi C, Chiarini F, Tabellini G, Ricci F, Tazzari PL, et al. (2012) AMP-dependent kinase/mammalian target of rapamycin complex 1 signaling in T-cell acute lymphoblastic leukemia: therapeutic implications. Leukemia 26: 91-100.
39. Martelli AM, Chiarini F, Evangelisti C, Ognibene A, Bressanin D, et al. (2012) Targeting the liver kinase B1/AMP-activated protein kinase pathway as a therapeutic strategy for hematological malignancies. Expert Opin Ther Targets 16: 729-742.
40. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, et al. Autophagy regulation by p53. Curr Opin Cell Biol 22: 181-185.
41. Kobayashi T, Ruan S, Jabbur JR, Consoli U, Clodi K, et al. (1998) Differential p53 phosphorylation and activation of apoptosis-promoting genes Bax and Fas/APO-1 by irradiation and ara-C treatment. Cell Death Differ 5: 584-591. (Pubitemid 28356580)
42. Bezombes C, Plo I, Mansat-De Mas V, Quillet-Mary A, Negre-Salvayre A, et al. (2001) Oxidative stress-induced activation of Lyn recruits sphingomyelinase and is requisite for its stimulation by Ara-C. Faseb J 15: 1583-1585.
43. Pham NA, Hedley DW (2001) Respiratory chain-generated oxidative stress following treatment of leukemic blasts with DNA-damaging agents. Exp Cell Res 264: 345-352.
44. Chen Y, Azad MB, Gibson SB (2009) Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 16: 1040-1052.
45. Li L, Chen Y, Gibson SB (2013) Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cell Signal 25: 50-65.
46. Li L, Ishdorj G, Gibson SB (2012) Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic Biol Med 53: 1399-1410.
47. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, et al. (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171: 603-614. (Pubitemid 41668720)
48. Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J (2008) Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 105: 20567-20574.
49. Kiffin R, Bandyopadhyay U, Cuervo AM (2006) Oxidative stress and autophagy. Antioxid Redox Signal 8: 152-162. (Pubitemid 43324542)
50. Cros E, Jordheim L, Dumontet C, Galmarini CM (2004) Problems related to resistance to cytarabine in acute myeloid leukemia. Leuk Lymphoma 45: 1123-1132. (Pubitemid 38584893)
51. Maycotte P, Aryal S, Cummings CT, Thorburn J, Morgan MJ, et al. (2012) Chloroquine sensitizes breast cancer cells to chemotherapy independent of autophagy. Autophagy 8: 200-212.
52. Martelli AM, Evangelisti C, Chappell W, Abrams SL, Basecke J, et al. (2011) Targeting the translational apparatus to improve leukemia therapy: roles of the PI3K/PTEN/Akt/mTOR pathway. Leukemia 25: 1064-1079.
53. Tett SE1, Cutler DJ, Day RO, Brown KF (1988) A dose-ranging study of the pharmacokinetics of hydroxy-chloroquine following intravenous administration to healthy volunteers. Br J Clin Pharmacol 26: 303-313.