Polyphenol tri-vanillic ester 13c inhibits P-JAK2V617F and Bcr-Abl oncokinase expression in correlation with STAT3/STAT5 inactivation and apoptosis induction in human leukemia cells

Cancer Letters

Volumn 340, Issue 1, 2013, Pages 30-42

  Trécul, Anne ^a   Morceau, Franck ^a   Gaigneaux, Anthoula ^a   Orsini, Marion ^a   Chateauvieux, Sébastien ^a   Grandjenette, Cindy ^a   Dicato, Mario ^a   Diederich, Marc ^b  

^a HÔpital Kirchberg   (Luxembourg)

^b Seoul National University   (South Korea)

Author keywords

13c; Bcr Abl; JAK2; Kinase; Polyphenol; STAT

Indexed keywords

ANTINEOPLASTIC AGENT; BCR ABL PROTEIN; JANUS KINASE 2; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P85; POLYPHENOL TRIVANILLIC ESTER 13C; PROTEIN MCL 1; PROTEIN TYROSINE KINASE; STAT3 PROTEIN; STAT5 PROTEIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MODIFICATION; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL LINE; LUNG ADENOCARCINOMA; MCL 1 GENE; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION;

13C; BCR-ABL; JAK2; KINASE; POLYPHENOL; STAT;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION; HUMANS; JANUS KINASE 2; K562 CELLS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; LEUKOCYTES, MONONUCLEAR; MUTATION, MISSENSE; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PARABENS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR;

EID: 84883772766     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.06.023     Document Type: Article

References (46)

1. Giovannini C., Masella R. Role of polyphenols in cell death control. Nutr. Neurosci. 2012, 15:134-149.
2. Esatbeyoglu T., Huebbe P., Ernst I.M., Chin D., Wagner A.E., Rimbach G. Curcumin - from molecule to biological function. Angew. Chem. 2012, 51:5308-5332.
3. Lamoral-Theys D., Wauthoz N., Heffeter P., Mathieu V., Jungwirth U., Lefranc F., Neve J., Dubois J., Dufrasne F., Amighi K., Berger W., Gailly P., Kiss R. Trivanillic polyphenols with anticancer cytostatic effects through the targeting of multiple kinases and intracellular Ca(2+) release. J. Cell. Mol. Med. 2011.
4. Ilaria R.L., Van Etten R.A. P210 and P190(BCR/ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J. Biol. Chem. 1996, 271:31704-31710.
5. Ozawa Y., Williams A.H., Estes M.L., Matsushita N., Boschelli F., Jove R., List A.F. Src family kinases promote AML cell survival through activation of signal transducers and activators of transcription (STAT). Leuk. Res. 2008, 32:893-903.
6. Epling-Burnette P.K., Liu J.H., Catlett-Falcone R., Turkson J., Oshiro M., Kothapalli R., Li Y., Wang J.M., Yang-Yen H.F., Karras J., Jove R., Loughran T.P. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J. Clin. Invest. 2001, 107:351-362.
7. Trecul A., Morceau F., Dicato M., Diederich M. Dietary compounds as potent inhibitors of the signal transducers and activators of transcription (STAT) 3 regulatory network. Genes Nutr. 2012, 7:111-125.
8. Baxter E.J., Scott L.M., Campbell P.J., East C., Fourouclas N., Swanton S., Vassiliou G.S., Bench A.J., Boyd E.M., Curtin N., Scott M.A., Erber W.N., Green A.R., Cancer Genome P. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 2005, 365:1054-1061.
9. James C., Ugo V., Casadevall N., Constantinescu S.N., Vainchenker W. A JAK2 mutation in myeloproliferative disorders: pathogenesis and therapeutic and scientific prospects. Trends Mol. Med. 2005, 11:546-554.
10. Kralovics R., Skoda R.C. Molecular pathogenesis of Philadelphia chromosome negative myeloproliferative disorders. Blood Rev. 2005, 19:1-13.
11. Levine R.L., Loriaux M., Huntly B.J., Loh M.L., Beran M., Stoffregen E., Berger R., Clark J.J., Willis S.G., Nguyen K.T., Flores N.J., Estey E., Gattermann N., Armstrong S., Look A.T., Griffin J.D., Bernard O.A., Heinrich M.C., Gilliland D.G., Druker B., Deininger M.W. The JAK2V617F activating mutation occurs in chronic myelomonocytic leukemia and acute myeloid leukemia, but not in acute lymphoblastic leukemia or chronic lymphocytic leukemia. Blood 2005, 106:3377-3379.
12. Choi B., Chun E., Kim S.Y., Kim M., Lee K.Y., Kim S.J. Notch-induced hIL-6 production facilitates the maintenance of self-renewal of hCD34+ cord blood cells through the activation of Jak-PI3K-STAT3 pathway. Am. J. Pathol. 2012, 180:351-364.
13. Gu F.M., Li Q.L., Gao Q., Jiang J.H., Huang X.Y., Pan J.F., Fan J., Zhou J. Sorafenib inhibits growth and metastasis of hepatocellular carcinoma by blocking STAT3. World J. Gastroenterol. 2011, 17:3922-3932.
14. Spiekermann K., Biethahn S., Wilde S., Hiddemann W., Alves F. Constitutive activation of STAT transcription factors in acute myelogenous leukemia. Eur. J. Haematol. 2001, 67:63-71.
15. Cortes J.E., Talpaz M., Beran M., O'Brien S.M., Rios M.B., Stass S., Kantarjian H.M. Philadelphia chromosome-negative chronic myelogenous leukemia with rearrangement of the breakpoint cluster region. Long-term follow-up results. Cancer 1995, 75:464-470.
16. Arana-Trejo R.M., Ruiz Sanchez E., Ignacio-Ibarra G., Baez de la Fuente E., Garces O., Gomez Morales E., Castro Granados M., Ovilla Martinez R., Rubio-Borja M.E., Solis Anaya L., Herrera P., Delgado Llamas J., Kofman S. BCR/ABL p210, p190 and p230 fusion genes in 250 Mexican patients with chronic myeloid leukaemia (CML). Clin. Lab. Haematol. 2002, 24:145-150.
17. Hantschel O., Nagar B., Guettler S., Kretzschmar J., Dorey K., Kuriyan J., Superti-Furga G. A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 2003, 112:845-857.
18. Deininger M.W., Goldman J.M., Melo J.V. The molecular biology of chronic myeloid leukemia. Blood 2000, 96:3343-3356.
19. Chatain N., Ziegler P., Fahrenkamp D., Jost E., Moriggl R., Schmitz-Van de Leur H., Muller-Newen G. Src family kinases mediate cytoplasmic retention of activated STAT5 in BCR-ABL-positive cells. Oncogene 2012.
20. Hoelbl A., Schuster C., Kovacic B., Zhu B., Wickre M., Hoelzl M.A., Fajmann S., Grebien F., Warsch W., Stengl G., Hennighausen L., Poli V., Beug H., Moriggl R., Sexl V. Stat5 is indispensable for the maintenance of bcr/abl-positive leukaemia. EMBO Mol. Med. 2010, 2:98-110.
21. Walz C., Ahmed W., Lazarides K., Betancur M., Patel N., Hennighausen L., Zaleskas V.M., Van Etten R.A. Essential role for Stat5a/b in myeloproliferative neoplasms induced by BCR-ABL1 and JAK2(V617F) in mice. Blood 2012, 119:3550-3560.
22. Chaturvedi P., Sharma S., Reddy E.P. Abrogation of interleukin-3 dependence of myeloid cells by the v-src oncogene requires SH2 and SH3 domains which specify activation of STATs. Mol. Cell. Biol. 1997, 17:3295-3304.
23. Lamoral-Theys D., Pottier L., Kerff F., Dufrasne F., Proutiere F., Wauthoz N., Neven P., Ingrassia L., Antwerpen P.V., Lefranc F., Gelbcke M., Pirotte B., Kraus J.L., Neve J., Kornienko A., Kiss R., Dubois J. Simple di- and trivanillates exhibit cytostatic properties toward cancer cells resistant to pro-apoptotic stimuli. Bioorg. Med. Chem. 2010, 18:3823-3833.
24. Schreiber E., Matthias P., Muller M.M., Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 1989, 17:6419.
25. Gao J., Ade A.S., Tarcea V.G., Weymouth T.E., Mirel B.R., Jagadish H.V., States D.J. Integrating and annotating the interactome using the MiMI plugin for cytoscape. Bioinformatics 2009, 25:137-138.
26. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
27. Blasius R., Reuter S., Henry E., Dicato M., Diederich M. Curcumin regulates signal transducer and activator of transcription (STAT) expression in K562 cells. Biochem. Pharmacol. 2006, 72:1547-1554.
28. Duvoix A., Morceau F., Delhalle S., Schmitz M., Schnekenburger M., Galteau M.M., Dicato M., Diederich M. Induction of apoptosis by curcumin: mediation by glutathione S-transferase P1-1 inhibition. Biochem. Pharmacol. 2003, 66:1475-1483.
29. Boengler K., Ungefug E., Heusch G., Schulz R. The STAT3 inhibitor Stattic Impairs cardiomyocyte mitochondrial function through increased reactive oxygen species formation. Curr. Pharm. Des. 2013.
30. Zhao W., Zhang T., Qu B., Wu X., Zhu X., Meng F., Gu Y., Shu Y., Shen Y., Sun Y., Xu Q. Sorafenib induces apoptosis in HL60 cells by inhibiting Src kinase-mediated STAT3 phosphorylation. Anticancer Drugs 2011, 22:79-88.
31. Argetsinger L.S., Kouadio J.L., Steen H., Stensballe A., Jensen O.N., Carter-Su C. Autophosphorylation of JAK2 on tyrosines 221 and 570 regulates its activity. Mol. Cell. Biol. 2004, 24:4955-4967.
32. Brasher B.B., Van Etten R.A. C-Abl has high intrinsic tyrosine kinase activity that is stimulated by mutation of the Src homology 3 domain and by autophosphorylation at two distinct regulatory tyrosines. J. Biol. Chem. 2000, 275:35631-35637.
33. Pluk H., Dorey K., Superti-Furga G. Autoinhibition of c-Abl. Cell 2002, 108:247-259.
34. Maloney A., Workman P. HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin. Biol. Ther. 2002, 2:3-24.
35. Nagar B., Hantschel O., Young M.A., Scheffzek K., Veach D., Bornmann W., Clarkson B., Superti-Furga G., Kuriyan J. Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell 2003, 112:859-871.
36. Morceau F., Buck I., Dicato M., Diederich M. Radicicol-mediated inhibition of Bcr-Abl in K562 cells induced p38-MAPK dependent erythroid differentiation and PU.1 down-regulation. Biofactors 2008, 34:313-329.
37. Nimmanapalli R., O'Bryan E., Bhalla K. Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res. 2001, 61:1799-1804.
38. Sawyers C.L., Callahan W., Witte O.N. Dominant negative MYC blocks transformation by ABL oncogenes. Cell 1992, 70:901-910.
39. Chang F., Steelman L.S., Lee J.T., Shelton J.G., Navolanic P.M., Blalock W.L., Franklin R.A., McCubrey J.A. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 2003, 17:1263-1293.
40. Junttila M.R., Puustinen P., Niemela M., Ahola R., Arnold H., Bottzauw T., Ala-aho R., Nielsen C., Ivaska J., Taya Y., Lu S.L., Lin S., Chan E.K., Wang X.J., Grenman R., Kast J., Kallunki T., Sears R., Kahari V.M., Westermarck J. CIP2A inhibits PP2A in human malignancies. Cell 2007, 130:51-62.
41. Choi H.J., Han J.S. Overexpression of phospholipase D enhances Bcl-2 expression by activating STAT3 through independent activation of ERK and p38MAPK in HeLa cells. Biochim. Biophys. Acta 1823, 2012:1082-1091.
42. Jiang L., Li Z., Rui L. Leptin stimulates both JAK2-dependent and JAK2-independent signaling pathways. J. Biol. Chem. 2008, 283:28066-28073.
43. Hamilton K.E., Simmons J.G., Ding S., Van Landeghem L., Lund P.K. Cytokine induction of tumor necrosis factor receptor 2 is mediated by STAT3 in colon cancer cells. Mol. Cancer Res. 2011, 9:1718-1731.
44. Lamontanara A.J., Gencer E.B., Kuzyk O., Hantschel O. Mechanisms of resistance to BCR-ABL and other kinase inhibitors. Biochim. Biophys. Acta 2012.
45. Dymock B.W., See C.S. Inhibitors of JAK2 and JAK3: an update on the patent literature 2010-2012. Expert Opin. Ther. Pat. 2013.
46. Verstovsek S. Ruxolitinib: an oral Janus kinase 1 and Janus kinase 2 inhibitor in the management of myelofibrosis. Postgrad. Med. 2013, 125:128-135.