Resveratrol promotes autophagic cell death in chronic myelogenous leukemia cells via JNK-mediated p62/SQSTM1 expression and AMPK activation

Cancer Research

Volumn 70, Issue 3, 2010, Pages 1042-1052

  Puissant, Alexandre ^a,b,d   Robert, Guillaume ^a,b,d   Fenouille, Nina ^a,b   Luciano, Frederic ^a,b,d   Cassuto, Jill Patrice ^c   Raynaud, Sophie ^c   Auberger, Patrick ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITY HOSPITAL OF NICE   (France)

^d Institute of Signalling Developmental Biology and Cancer Research   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMATINIB; MAMMALIAN TARGET OF RAPAMYCIN; PHYTOALEXIN; PROTEIN P62; RESVERATROL; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CELL VIABILITY; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID CHLOROMETHYL KETONES; AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; AUTOPHAGY; BLOTTING, WESTERN; CASPASES; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MACROLIDES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; PIPERAZINES; PYRIMIDINES; RNA INTERFERENCE; STILBENES; TUMOR CELLS, CULTURED; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 76249124608     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-3537     Document Type: Article

References (47)

1. Clarkson B, Strife A. Linkage of proliferative and maturational abnormalities in chronic myelogenous leukemia and relevance to treatment. Leukemia 1993;7:1683-721.
2. Groffen J, Stephenson JR, Heisterkamp N, de Klein A, Bartram CR, Grosveld G. Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22. Cell 1984; 36:93-9.
3. Ren R. The molecular mechanism of chronic myelogenous leukemia and its therapeutic implications: studies in a murine model. Oncogene 2002;21:8629-42.
4. Deininger MW, Goldman JM, Melo JV. The molecular biology of chronic myeloid leukemia. Blood 2000;96:3343-56.
5. Jacquel A, Herrant M, Defamie V, et al. A survey of the signaling pathways involved in megakaryocytic differentiation of the human K562 leukemia cell line by molecular and c-DNA array analysis. Oncogene 2006;25:781-94.
6. Steelman LS, Pohnert SC, Shelton JG, Franklin RA, Bertrand FE, McCubrey JA. JAK/STAT, Raf/MEK/ERK, PI3K/Akt and BCR-ABL in cell cycle progression and leukemogenesis. Leukemia 2004;18: 189-218.
7. Shen M, Jia GL, Wang YM, Ma H. Cardioprotective effect of resvaratrol pretreatment on myocardial ischemia-reperfusion induced injury in rats. Vascul Pharmacol 2006;45:122-6, Epub 2006 Jun 12.
8. Athar M, Back JH, Tang X, et al. Resveratrol: a review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 2007;3:3.
9. Gao X, Xu YX, Divine G, Janakiraman N, Chapman RA, Gautam SC. Disparate in vitro and in vivo antileukemic effects of resveratrol, a natural polyphenolic compound found in grapes. J Nutr 2002;132: 2076-81.
10. MacCarrone M, Lorenzon T, Guerrieri P, Agro AF. Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity. Eur J Biochem 1999;265:27-34.
11. Luzi C, Brisdelli F, Cinque B, Cifone G, Bozzi A. Differential sensitivity to resveratrol-induced apoptosis of human chronic myeloid (K562) and acute lymphoblastic (HSB-2) leukemia cells. Biochem Pharmacol 2004;68:2019-30.
12. Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008;4:151-75.
13. Puissant A, Grosso S, Jacquel A, et al. Imatinib mesylate-resistant human chronic myelogenous leukemia cell lines exhibit high sensitivity to the phytoalexin resveratrol. FASEB J 2008;5:5.
14. Marino G, Lopez-Otin C. Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci 2004;61:1439-54.
15. Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: targeting autophagy signalling in cancer cells - 'trick or treats'? FEBS J 2009;276:6084-96.
16. Maiuri MC, Tasdemir E, Criollo A, et al. Control of autophagy by oncogenes and tumor suppressor genes. Cell Death Differ 2009;16:87-93.
17. Kroemer G, Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005;5:886-97.
18. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and selfkilling: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007;8:741-52.
19. Hsu KF, Wu CL, Huang SC, et al. Cathepsin L mediates resveratrolinduced autophagy and apoptotic cell death in cervical cancer cells. Autophagy 2009;5:451-60.
20. Ohshiro K, Rayala SK, Kondo S, et al. Identifying the estrogen receptor coactivator PELP1 in autophagosomes. Cancer Res 2007;67: 8164-71.
21. Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 2008;15:1318-29.
22. Signorelli P, Munoz-Olaya JM, Gagliostro V, Casas J, Ghidoni R, Fabrias G. Dihydroceramide intracellular increase in response to resveratrol treatment mediates autophagy in gastric cancer cells. Cancer Lett 2009;282:238-43.
23. Trincheri NF, Nicotra G, Follo C, Castino R, Isidoro C. Resveratrol induces cell death in colorectal cancer cells by a novel pathway involving lysosomal cathepsin D. Carcinogenesis 2007;28:922-31.
24. Grosso S, Puissant A, Dufies M, et al. Gene expression profiling of imatinib and PD166326-resistant CML cell lines identifies Fyn as a gene associated with resistance to BCR-ABL inhibitors. Mol Cancer Ther 2009;8:1924-33.
25. Jacquel A, Colosetti P, Grosso S, et al. Apoptosis and erythroid differentiation triggered by Bcr-Abl inhibitors in CML cell lines are fully distinguishable processes that exhibit different sensitivity to caspase inhibition. Oncogene 2007;26:2445-58, Epub 006 Oct 9.
26. Mahon FX, Deininger MW, Schultheis B, et al. Selection and characterization of BCR-ABL positive cell lines with differential sensitivity to the tyrosine kinase inhibitor STI571: diverse mechanisms of resistance. Blood 2000;96:1070-9.
27. Colosetti P, Puissant A, Robert G, et al. Autophagy is an important event for megakaryocytic differentiation of the chronic myelogenous leukemia K562 cell line. Autophagy 2009;5:1092-8.
28. Jacquel A, Herrant M, Legros L, et al. Imatinib induces mitochondriadependent apoptosis of the Bcr-Abl-positive K562 cell line and its differentiation toward the erythroid lineage. FASEB J 2003;17: 2160-2.
29. Baur JA, Pearson KJ, Price NL, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006;444: 337-42.
30. Dasgupta B, Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 2007;104:7217-22.
31. Ben Sahra I, Laurent K, Loubat A, et al. The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene 2008;27:3576-86.
32. Kundu JK, Surh YJ. Cancer chemopreventive and therapeutic potential of resveratrol: mechanistic perspectives. Cancer Lett 2008;269: 243-61.
33. Ogata M, Hino S, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006;26: 9220-31.
34. Li DD, Wang LL, Deng R, et al. The pivotal role of c-Jun NH2-terminal kinase-mediated Beclin 1 expression during anticancer agentsinduced autophagy in cancer cells. Oncogene 2009;28:886-98.
35. She QB, Huang C, Zhang Y, Dong Z. Involvement of c-jun NH(2)-terminal kinases in resveratrol-induced activation of p53 and apoptosis. Mol Carcinog 2002;33:244-50.
36. Su JL, Lin MT, Hong CC, et al. Resveratrol induces FasL-related apoptosis through Cdc42 activation of ASK1/JNK-dependent signaling pathway in human leukemia HL-60 cells. Carcinogenesis 2005; 26:1-10.
37. Aquilano K, Baldelli S, Rotilio G, Ciriolo MR. trans-Resveratrol inhibits H2O2-induced adenocarcinoma gastric cells proliferation via inactivation of MEK1/2-ERK1/2-c-Jun signalling axis. Biochem Pharmacol 2009;77:337-47.
38. Woo JH, Lim JH, Kim YH, et al. Resveratrol inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting JNK and PKC δ signal transduction. Oncogene 2004;23:1845-53.
39. Lorin S, Borges A, Ribeiro Dos Santos L, et al. c-Jun NH2-terminal kinase activation is essential for DRAM-dependent induction of autophagy and apoptosis in 2-methoxyestradiol-treated Ewing sarcoma cells. Cancer Res 2009;69:6924-31.
40. Park KJ, Lee SH, Lee CH, et al. Upregulation of Beclin-1 expression and phosphorylation of Bcl-2 and p53 are involved in the JNKmediated autophagic cell death. Biochem Biophys Res Commun 2009;382:726-9.
41. Lee YH, Ko J, Joung I, Kim JH, Shin J. Immediate early response of the p62 gene encoding a non-proteasomal multiubiquitin chain binding protein. FEBS Lett 1998;438:297-300.
42. Geetha T, Wooten MW. Structure and functional properties of the ubiquitin binding protein p62. FEBS Lett 2002;512:19-24.
43. Wooten MW, Geetha T, Babu JR, et al. Essential role of sequestosome 1/p62 in regulating accumulation of Lys63-ubiquitinated proteins. J Biol Chem 2008;283:6783-9.
44. Duran A, Linares JF, Galvez AS, et al. The signaling adaptor p62 is an important NF-κB mediator in tumorigenesis. Cancer Cell 2008;13: 343-54.
45. Mathew R, Karp CM, Beaudoin B, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009;137:1062-75.
46. Morotti A, Cilloni D, Pautasso M, et al. NF-̂B inhibition as a strategy to enhance etoposide-induced apoptosis in K562 cell line. Am J Hematol 2006;81:938-45.
47. Hsieh TC, Lu X, Wang Z, Wu JM. Induction of quinone reductase NQO1 by resveratrol in human K562 cells involves the antioxidant response element ARE and is accompanied by nuclear translocation of transcription factor Nrf2. Med Chem 2006;2:275-85.