ABT-737 resistance in B-cells isolated from chronic lymphocytic leukemia patients and leukemia cell lines is overcome by the pleiotropic kinase inhibitor quercetin through Mcl-1 down-regulation

Biochemical Pharmacology

Volumn 85, Issue 7, 2013, Pages 927-936

  Russo, Maria ^a   Spagnuolo, Carmela ^a   Volpe, Silvestro ^b   Tedesco, Idolo ^a   Bilotto, Stefania ^a   Russo, Gian Luigi ^a  

^a CNR   (Italy)

^b S G MOSCATI HOSPITAL   (Italy)

Author keywords

ABT 737; Apoptosis; Chronic lymphocytic leukemia; Mcl 1; Quercetin

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN MCL 1; QUERCETIN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CANCER RESISTANCE; CELL ISOLATION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG POTENTIATION; DRUG SENSITIVITY; HUMAN; HUMAN CELL; LEUKEMIA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; APOPTOSIS; B-LYMPHOCYTES; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HUMANS; LEUKEMIA; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NITROPHENOLS; PHOSPHATIDYLINOSITOL 3-KINASES; PIPERAZINES; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; QUERCETIN; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 84874657510     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.01.011     Document Type: Article

References (53)

1. G. Dighiero, and T.J. Hamblin Chronic lymphocytic leukaemia Lancet 371 2008 1017 1029 (Pubitemid 351389535)
2. K. Abou-Nassar, and J.R. Brown Novel agents for the treatment of chronic lymphocytic leukemia Clin Adv Hematol Oncol 8 2010 886 895
3. M. Hallek Therapy of chronic lymphocytic leukaemia Best Pract Res Clin Haematol 23 2010 85 96
4. K.W. Yee, and S.M. O'Brien Chronic lymphocytic leukemia: diagnosis and treatment Mayo Clin Proc 81 2006 1105 1129 (Pubitemid 44175023)
5. T. Elter, L. Gercheva-Kyuchukova, H. Pylylpenko, T. Robak, B. Jaksic, and G. Rekhtman Fludarabine plus alemtuzumab versus fludarabine alone in patients with previously treated chronic lymphocytic leukaemia: a randomised phase 3 trial Lancet Oncol 12 2011 1204 1213
6. K. Lu, and X. Wang Therapeutic advancement of chronic lymphocytic leukemia J Hematol Oncol 5 2012 55
7. A.G. Buggins, and C.J. Pepper The role of Bcl-2 family proteins in chronic lymphocytic leukaemia Leuk Res 34 2010 837 842
8. S.L. Khaw, D.C. Huang, and A.W. Roberts Overcoming blocks in apoptosis with BH3-mimetic therapy in haematological malignancies Pathology 43 2011 525 535
9. T. Oltersdorf, S.W. Elmore, A.R. Shoemaker, R.C. Armstrong, D.J. Augeri, and B.A. Belli An inhibitor of Bcl-2 family proteins induces regression of solid tumours Nature 435 2005 677 681 (Pubitemid 40825512)
10. C. Tse, A.R. Shoemaker, J. Adickes, M.G. Anderson, J. Chen, and S. Jin ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor Cancer Res 68 2008 3421 3428
11. L.E. Robertson, W. Plunkett, K. McConnell, M.J. Keating, and T.J. McDonnell Bcl-2 expression in chronic lymphocytic leukemia and its correlation with the induction of apoptosis and clinical outcome Leukemia 10 1996 456 459 (Pubitemid 26128784)
12. J.M. Tromp, C.R. Geest, E.C. Breij, J.A. Elias, J. van Laar, and D.M. Luijks Tipping the Noxa/Mcl-1 balance overcomes ABT-737 resistance in chronic lymphocytic leukemia Clin Cancer Res 18 2012 487 498
13. S.K. Tahir, X. Yang, M.G. Anderson, S.E. Morgan-Lappe, A.V. Sarthy, and J. Chen Influence of Bcl-2 family members on the cellular response of small-cell lung cancer cell lines to ABT-737 Cancer Res 67 2007 1176 1183
14. M.F. van Delft, A.H. Wei, K.D. Mason, C.J. Vandenberg, L. Chen, and P.E. Czabotar The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized Cancer Cell 10 2006 389 399 (Pubitemid 44711953)
15. S. Al-Harbi, B.T. Hill, S. Mazumder, K. Singh, J. Devecchio, and G. Choudhary An antiapoptotic BCL-2 family expression index predicts the response of chronic lymphocytic leukemia to ABT-737 Blood 118 2011 3579 3590
16. L. Veronese, O. Tournilhac, P. Verrelle, F. Davi, G. Dighiero, and E. Chautard Low MCL-1 mRNA expression correlates with prolonged survival in B-cell chronic lymphocytic leukemia Leukemia 22 2008 1291 1293 (Pubitemid 351833810)
17. S. Derenne, B. Monia, N.M. Dean, J.K. Taylor, M.J. Rapp, and J.L. Harousseau Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-x(l) is an essential survival protein of human myeloma cells Blood 100 2002 194 199 (Pubitemid 35177447)
18. S.R. Hussain, C.M. Cheney, A.J. Johnson, T.S. Lin, M.R. Grever, and M.A. Caligiuri Mcl-1 is a relevant therapeutic target in acute and chronic lymphoid malignancies: down-regulation enhances rituximab-mediated apoptosis and complement-dependent cytotoxicity Clin Cancer Res 13 2007 2144 2150 (Pubitemid 46649884)
19. J. Michels, J.W. O'Neill, C.L. Dallman, A. Mouzakiti, F. Habens, and M. Brimmell Mcl-1 is required for Akata6 B-lymphoma cell survival and is converted to a cell death molecule by efficient caspase-mediated cleavage Oncogene 23 2004 4818 4827 (Pubitemid 38932154)
20. C. Pepper, and C. Fegan CLL: a supplementary question? Blood 117 2011 1439 1440
21. P.G. Longo, L. Laurenti, S. Gobessi, S. Sica, G. Leone, and D.G. Efremov The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells Blood 111 2008 846 855
22. A. Petlickovski, L. Laurenti, X. Li, S. Marietti, P. Chiusolo, and S. Sica Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells Blood 105 2005 4820 4827 (Pubitemid 40807309)
23. D.W. Lamson, and M.S. Brignall Antioxidants and cancer, part 3: quercetin Altern Med Rev 5 2000 196 208
24. C. Spagnuolo, C. Cerella, M. Russo, S. Chateauvieux, M. Diederich, and G.L. Russo Quercetin downregulates Mcl-1 by acting on mRNA stability and protein degradation Br J Cancer 105 2011 221 230
25. M. Daker, M. Ahmad, and A.S. Khoo Quercetin-induced inhibition and synergistic activity with cisplatin-a chemotherapeutic strategy for nasopharyngeal carcinoma cells Cancer Cell Int 12 2012 34
26. M. Russo, C. Spagnuolo, I. Tedesco, S. Bilotto, and G.L. Russo The flavonoid quercetin in disease prevention and therapy: facts and fancies Biochem Pharmacol 83 2012 6 15
27. M. Russo, P. Nigro, R. Rosiello, R. D'Arienzo, and G.L. Russo Quercetin enhances CD95- and TRAIL-induced apoptosis in leukemia cell lines Leukemia 21 2007 1130 1133 (Pubitemid 46672100)
28. M. Russo, R. Palumbo, A. Mupo, M. Tosto, G. Iacomino, and A. Scognamiglio Flavonoid quercetin sensitizes a CD95-resistant cell line to apoptosis by activating protein kinase Calpha Oncogene 22 2003 3330 3342 (Pubitemid 36717126)
29. M. Russo, R. Palumbo, I. Tedesco, G. Mazzarella, P. Russo, and G. Iacomino Quercetin and anti-CD95(Fas/Apo1) enhance apoptosis in HPB-ALL cell line FEBS Lett 462 1999 322 328
30. M. Russo, C. Spagnuolo, S. Volpe, A. Mupo, I. Tedesco, and G.L. Russo Quercetin induced apoptosis in association with death receptors and fludarabine in cells isolated from chronic lymphocytic leukaemia patients Br J Cancer 103 2010 642 648
31. Y. Bomstein, M. Yuklea, J. Radnay, H. Shapiro, F. Afanasyev, and S. Yarkoni The antiapoptotic effects of blood constituents in patients with chronic lymphocytic leukemia Eur J Haematol 70 2003 290 295 (Pubitemid 36560526)
32. T.C. Chou, and P. Talalay Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors Adv Enzyme Regul 22 1984 27 55
33. S. Chen, Y. Dai, H. Harada, P. Dent, and S. Grant Mcl-1 down-regulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation Cancer Res 67 2007 782 791 (Pubitemid 46192219)
34. F.T. Awan, N.E. Kay, M.E. Davis, W. Wu, S.M. Geyer, and N. Leung Mcl-1 expression predicts progression-free survival in chronic lymphocytic leukemia patients treated with pentostatin, cyclophosphamide, and rituximab Blood 113 2009 535 537
35. S. Kitada, and J.C. Reed MCL-1 promoter insertions dial-up aggressiveness of chronic leukemia J Natl Cancer Inst 96 2004 642 643 (Pubitemid 38660217)
36. M. Vogler, M. Butterworth, A. Majid, R.J. Walewska, X.M. Sun, and M.J. Dyer Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia Blood 113 2009 4403 4413
37. S. Cheng, N. Gao, Z. Zhang, G. Chen, A. Budhraja, and Z. Ke Quercetin induces tumor-selective apoptosis through downregulation of Mcl-1 and activation of Bax Clin Cancer Res 16 2010 5679 5691
38. J.T. Opferman Unraveling MCL-1 degradation Cell Death Differ 13 2006 1260 1262 (Pubitemid 44057455)
39. L.W. Thomas, C. Lam, and S.W. Edwards Mcl-1; the molecular regulation of protein function FEBS Lett 584 2010 2981 2989
40. D.X. Hou, and T. Kumamoto Flavonoids as protein kinase inhibitors for cancer chemoprevention: direct binding and molecular modeling Antioxid Redox Signal 13 2010 691 719
41. M.K. Hwang, N.R. Song, N.J. Kang, K.W. Lee, and H.J. Lee Activation of phosphatidylinositol 3-kinase is required for tumor necrosis factor-alpha-induced upregulation of matrix metalloproteinase-9: its direct inhibition by quercetin Int J Biochem Cell Biol 41 2009 1592 1600
42. K.W. Lee, N.J. Kang, Y.S. Heo, E.A. Rogozin, A. Pugliese, and M.K. Hwang Raf and MEK protein kinases are direct molecular targets for the chemopreventive effect of quercetin, a major flavonol in red wine Cancer Res 68 2008 946 955 (Pubitemid 351206774)
43. D. Yecies, N.E. Carlson, J. Deng, and A. Letai Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1 Blood 115 2010 3304 3313
44. Q. Zhong, W. Gao, F. Du, and X. Wang Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis Cell 121 2005 1085 1095 (Pubitemid 40884398)
45. M. Vogler, S.D. Furdas, M. Jung, T. Kuwana, M.J. Dyer, and G.M. Cohen Diminished sensitivity of chronic lymphocytic leukemia cells to ABT-737 and ABT-263 due to albumin binding in blood Clin Cancer Res 16 2010 4217 4225
46. V. Del Gaizo Moore, J.R. Brown, M. Certo, T.M. Love, C.D. Novina, and A. Letai Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737 J Clin Invest 117 2007 112 121 (Pubitemid 46048458)
47. M. Vogler, K. Weber, D. Dinsdale, I. Schmitz, K. Schulze-Osthoff, and M.J. Dyer Different forms of cell death induced by putative BCL2 inhibitors Cell Death Differ 16 2009 1030 1039
48. A.W. Roberts, J.F. Seymour, J.R. Brown, W.G. Wierda, T.J. Kipps, and S.L. Khaw Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease J Clin Oncol 30 2012 488 496
49. D.R. Ferry, A. Smith, J. Malkhandi, D.W. Fyfe, P.G. deTakats, and D. Anderson Phase I clinical trial of the flavonoid quercetin: pharmacokinetics and evidence for in vivo tyrosine kinase inhibition Clin Cancer Res 2 1996 659 668 (Pubitemid 26133468)
50. G.L. Russo Ins and outs of dietary phytochemicals in cancer chemoprevention Biochem Pharmacol 74 2007 533 544 (Pubitemid 47042006)
51. E.H. Walker, M.E. Pacold, O. Perisic, L. Stephens, P.T. Hawkins, and M.P. Wymann Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine Mol Cell 6 2000 909 919
52. A.N. Howard, K.A. Bridges, R.E. Meyn, and J. Chandra ABT-737, a BH3 mimetic, induces glutathione depletion and oxidative stress Cancer Chemother Pharmacol 65 2009 41 54
53. T.D. Shanafelt, M.T. Drake, M.J. Maurer, C. Allmer, K.G. Rabe, and S.L. Slager Vitamin D insufficiency and prognosis in chronic lymphocytic leukemia Blood 117 2011 1492 1498