Vinblastine sensitizes leukemia cells to cyclin-dependent kinase inhibitors, inducing acute cell cycle phase-independent apoptosis

Cancer Biology and Therapy

Volumn 12, Issue 4, 2011, Pages 314-325

  Bates, Darcy J P ^a   Salerni, Bethany L ^a   Lowrey, Christopher H ^a   Eastman, Alan ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

c Jun N terminal kinase; Dinaciclib; Flavopiridol; Mcl 1; Vinblastine

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CYCLIN DEPENDENT KINASE INHIBITOR; DINACICLIB; FLAVOPIRIDOL; PACLITAXEL; VINBLASTINE;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL CYCLE; CELL ISOLATION; CHRONIC LEUKEMIA; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG SENSITIZATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHOCYTE;

ANTHRACENES; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE 9; CYCLIN-DEPENDENT KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FLAVONOIDS; HL-60 CELLS; HUMANS; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; JURKAT CELLS; PACLITAXEL; PIPERIDINES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIDINIUM COMPOUNDS; U937 CELLS; VINBLASTINE;

EID: 84860405325     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.12.4.16909     Document Type: Article

References (36)

1. Townsend K.J., Zhou P., Qian L., Bieszczad C.K., Lowrey C.H., Yen A., et al. Regulation of MCL1 through a serum response factor/Elk-1-mediated mechanism links expression of a viability-promoting member of the BCL2 family to the induction of hematopoietic cell differentiation. J Biol Chem 1999; 274:1801-13; PMID: 9880563; DOI: 10.1074/jbc.274.3.1801.
2. Stadheim T.A., Xiao H., Eastman A. Inhibition of extracellular signal-regulated kinase (ERK) mediates cell cycle phase independent apoptosis in vinblastine-treated ML-1 cells. Cancer Res 2001; 61:1533-1540; PMID: 11245462.
3. Salerni B.L., Bates D.J., Albershardt T.C., Lowrey C.H., Eastman A Vinblastine induces acute, cell cycle phase-independent apoptosis in some leukemias and lymphomas and can induce acute apoptosis in others when Mcl-1 is suppressed Mol Cancer Ther 2010; 9:791-802; PMID: 20371726; DOI: 10.1158/1535-7163. MCT-10-0028.
4. Losiewicz M.D., Carlson B.A., Kaur G., Sausville E.A., Worland PJ Potent inhibition of CDC2 kinase activity by the flavonoid L86-8275 Biochem Biophys Res Commun 1994; 201:589-95; PMID: 8002990; DOI: 10.1006/bbrc.1994.1742.
5. Chao S.H., Fujinaga K., Marion J.E., Taube R., Sausville E.A., Senderowicz A.M., et al. Flavopiridol inhibits P-TEFb and blocks HIV-1 replication. J Biol Chem 2000; 275:28345-8; PMID: 10906320; DOI: 10.1074/jbc.C000446200.
6. Chao S.H., Price DH Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo J Biol Chem 2001; 276:31793-9; PMID: 11431468; DOI: 10.1074/jbc.M102306200.
7. Lam L.T., Pickeral O.K., Peng A.C., Rosenwald A., Hurt E.M., Giltnane J.M., et al. Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol 2001; 2:41.
8. De Azevedo W.F. Jr, Canduri F., da Silveira NJ Structural basis for inhibition of cyclin-dependent kinase 9 by flavopiridol Biochem Biophys Res Commun 2002; 293:566-71; PMID: 12054639; DOI: 10.1016/S0006-291X(02)00266-8.
9. Lu X., Burgan W.E., Cerra M.A., Chuang E.Y., Tsai M.H., Tofilon P.J., et al. Transcriptional signature of flavopiridol- induced tumor cell death. Mol Cancer Ther 2004; 3:861-872; PMID: 15252147.
10. Chen R., Keating M.J., Gandhi V., Plunkett W Transcription inhibition by flavopiridol: mechanism of chronic lymphocytic leukemia cell death Blood 2005; 106:2513-9; PMID: 15972445; DOI: 10.1182/blood-2005-04-1678.
11. Byrd J.C., Shinn C., Waselenko J.K., Fuchs E.J., Lehman T.A., Nguyen P.L., et al. Flavopiridol induces apoptosis in chronic lymphocytic leukemia cells via activation of caspase-3 without evidence of bcl-2 modulation or dependence on functional p53. Blood 1998; 92:3804-3816; PMID: 9808574.
12. Kitada S., Zapata J.M., Andreeff M., Reed J.C. Protein kinase inhibitors flavopiridol and 7-hydroxy-staurosporine downregulate antiapoptosis proteins in B-cell chronic lymphocytic leukemia. Blood 2000; 96:393-397; PMID: 10887097.
13. Pepper C., Thomas A., Hoy T., Fegan C., Bentley P Flavopiridol circumvents Bcl-2 family mediated inhibition of apoptosis and drug resistance in B-cell chronic lymphocytic leukaemia Br J Haematol 2001; 114:70-7; PMID: 11472347; DOI: 10.1046/j.1365-2141.2001.02895.x.
14. Ma Y., Cress W.D., Haura E.B. Flavopiridol-induced apoptosis is mediated through upregulation of E2F1 and repression of Mcl-1. Mol Cancer Ther 2003; 2:73-81; PMID: 12533675.
15. Lin T.S., Ruppert A.S., Johnson A.J., Fischer B., Heerema N.A., Andritsos L.A., et al. Phase II study of flavopiridol in relapsed chronic lymphocytic leukemia demonstrating high response rates in genetically high-risk disease. J Clin Oncol 2009; 27:6012-8; PMID: 19826119; DOI: 10.1200/JCO.2009.22.6944.
16. Rosato R.R., Almenara J.A., Kolla S.S., Maggio S.C., Coe S., Gimenez M.S., et al. Mechanism and functional role of XIAP and Mcl-1 downregulation in flavopiridol/ vorinostat antileukemic interactions. Mol Cancer Ther 2007; 6:692-702; PMID: 17308065; DOI: 10.1158/1535-7163.MCT-06-0562.
17. Parry D., Guzi T., Shanahan F., Davis N., Prabhavalkar D., Wiswell D., et al. Dinaciclib (SCH 727965), a novel and potent cyclin-dependent kinase inhibitor. Mol Cancer Ther 2010; 9:2344-53; PMID: 20663931; DOI: 10.1158/1535-7163.MCT-10-0324.
18. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., Chen S.L., et al. Ribotoxic stress response: Activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ ricin loop in the 28S rRNA. Mol Cell Biol 1997; 17:3373-3381; PMID: 9154836.
19. Byrd J.C., Peterson B.L., Gabrilove J., Odenike O.M., Grever M.R., Rai K., et al. Treatment of relapsed chronic lymphocytic leukemia by 72-hour continuous infusion or 1-hour bolus infusion of flavopiridol: results from Cancer and Leukemia Group B study 19,805. Clin Cancer Res 2005; 11:4176-81; PMID: 15930354; DOI: 10.1158/1078-0432.CCR-04-2276.
20. Phelps M.A., Lin T.S., Johnson A.J., Hurh E., Rozewski D.M., Farley K.L., et al. Clinical response and pharmacokinetics from a phase 1 study of an active dosing schedule of flavopiridol in relapsed chronic lymphocytic leukemia. Blood 2009; 113:2637-45; PMID: 18981292; DOI: 10.1182/blood-2008-07-168583.
21. Flynn J.M., Johnson A.J., Andritsos L.A., Blum K.A., Jones J.A., Wiley E.A., et al. The cyclin dependent kinase inhibitor SCH 727965 demonstrates promising preclinical and early clinical activitiy in chronic lymphocytic leukemia. Abstract 51st ASH Annual Meeting and Exposition 2009.
22. Garriga J., Grana X Cellular control of gene expression by T-type cyclin/CDK9 complexes Gene 2004; 337:15-23; PMID: 15276198; DOI: 10.1016/j.gene.2004.05.007.
23. Hussain S.R., Lucas D.M., Johnson A.J., Lin T.S., Bakaletz A.P., Dang V.X., et al. Flavopiridol causes early mitochondrial damage in chronic lymphocytic leukemia cells with impaired oxygen consumption and mobilization of intracellular calcium. Blood 2008; 111:3190-9; PMID: 18192508; DOI: 10.1182/blood-2007-10-115733.
24. Rosato R.R., Dai Y., Almenara J.A., Maggio S.C., Grant S Potent antileukemic interactions between flavopiridol and TRAIL/Apo2L involve flavopiridol-mediated XIAP downregulation Leukemia 2004; 18:1780-8; PMID: 15385934; DOI: 10.1038/sj.leu.2403491.
25. Yamamoto K., Ichijo H., Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol Cell Biol 1999; 19:8469-8478; PMID: 10567572.
26. Fan M., Goodwin M., Vu T., Brantley-Finley C., Gaarde W.A., Chambers TC Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ ERK cascade J Biol Chem 2000; 275:29980-5; PMID: 10913135; DOI: 10.1074/jbc.M003776200.
27. Fan M., Goodwin M.E., Birrer M.J., Chambers T.C. The c-Jun NH(2)-terminal protein kinase/AP-1 pathway is required for efficient apoptosis induced by vinblastine. Cancer Res 2001; 61:4450-4458; PMID: 11389075.
28. Muscarella D.E., Bloom SE The contribution of c-Jun N-terminal kinase activation and subsequent Bcl-2 phosphorylation to apoptosis induction in human B-cells is dependent on the mode of action of specific stresses Toxicol Appl Pharmacol 2008; 228:93-104; PMID: 18201741; DOI: 10.1016/j.taap.2007.11.032.
29. Kharbanda S., Saxena S., Yoshida K., Pandey P., Kaneki M., Wang Q., et al. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J Biol Chem 2000; 275:322-7; PMID: 10617621; DOI: 10.1074/jbc.275.1.322.
30. Inoshita S., Takeda K., Hatai T., Terada Y., Sano M., Hata J., et al. Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 2002; 277:43730-4; PMID: 12223490; DOI: 10.1074/jbc.M207951200.
31. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., et al. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J 2004; 23:1889-99; PMID: 15071501; DOI: 10.1038/sj.emboj.7600194.
32. Sunayama J., Tsuruta F., Masuyama N., Gotoh Y JNK antagonizes Akt-mediated survival signals by phosphorylating 14-3-3 J Cell Biol 2005; 170:295-304; PMID: 16009721; DOI: 10.1083/jcb.200409117.
33. Putcha G.V., Le S., Frank S., Besirli C.G., Clark K., Chu B., et al. JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron 2003; 38:899-914; PMID: 12818176; DOI: 10.1016/S0896-6273(03)00355-6.
34. Rudek M.A., Bauer K.S. Jr, Lush R.M., 3rd, Stinson S.F., Senderowicz A.M., Headlee D.J., et al. Clinical pharmacology of flavopiridol following a 72-hour continuous infusion. Ann Pharmacother 2003; 37:1369-74; PMID: 14519054; DOI: 10.1345/aph.1C404.
35. Senderowicz A.M., Headlee D., Stinson S.F., Lush R.M., Kalil N., Villalba L., et al. Phase I trial of continuous infusion flavopiridol, a novel cyclin-dependent kinase inhibitor, in patients with refractory neoplasms. J Clin Oncol 1998; 16:2986-2999; PMID: 9738567.
36. Senderowicz A.M., Sausville EA Preclinical and clinical development of cyclin-dependent kinase modulators J Natl Cancer Inst 2000; 92:376-87; PMID: 10699068; DOI: 10.1093/jnci/92.5.376.