Molecular targeting of MLL-rearranged leukemia cell lines with the synthetic peptide PFWT synergistically enhances the cytotoxic effect of established chemotherapeutic agents

Leukemia Research

Volumn 33, Issue 7, 2009, Pages 937-947

  Bennett, Cecily A ^a   Winters, Amanda C ^b   Barretto, Nisha N ^c   Hemenway, Charles S ^d  

^a TULANE UNIVERSITY   (United States)

^b TULANE UNIVERSITY   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d LOYOLA UNIVERSITY HEALTH SYSTEM   (United States)

Author keywords

Apoptosis; Drug synergy; MLL; Necrosis; Peptide therapeutics

Indexed keywords

CYTARABINE; ETOPOSIDE; MIXED LINEAGE LEUKEMIA PROTEIN;

APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CLONOGENESIS; CONTROLLED STUDY; CYTOGENETICS; CYTOTOXICITY; GENE TRANSLOCATION; HUMAN; HUMAN CELL; LEUKEMIA; LEUKEMIA CELL LINE; PRIORITY JOURNAL;

ANTIMETABOLITES, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; CHROMOSOMES, HUMAN, PAIR 11; CHROMOSOMES, HUMAN, PAIR 4; CHROMOSOMES, HUMAN, PAIR 9; COLONY-FORMING UNITS ASSAY; CYTARABINE; DNA-BINDING PROTEINS; DRUG SYNERGISM; ETOPOSIDE; GENE REARRANGEMENT; HUMANS; LEUKEMIA; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NECROSIS; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; TRANSLOCATION, GENETIC; TUMOR CELLS, CULTURED;

EID: 67349158014     PISSN: 01452126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.leukres.2009.01.018     Document Type: Article

References (50)

1. Daser A., and Rabbitts T.H. Extending the repertoire of the mixed-lineage leukemia gene MLL in leukemogenesis. Genes Dev 18 9 (2004) 965-974
2. Biondi A., Cimino G., Pieters R., and Pui C.H. Biological and therapeutic aspects of infant leukemia. Blood 96 1 (2000) 24-33
3. Pui C.H., Gaynon P.S., Boyett J.M., Chessells J.M., Baruchel A., Kamps W., et al. Outcome of treatment in childhood acute lymphoblastic leukaemia with rearrangements of the 11q23 chromosomal region. Lancet 359 9321 (2002) 1909-1915
4. Nakamura T., Mori T., Tada S., Krajewski W., Rozovskaia T., Wassell R., et al. ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol Cell 10 5 (2002) 1119-1128
5. Yokoyama A., Wang Z., Wysocka J., Sanyal M., Aufiero D.J., Kitabayashi I., et al. Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 24 13 (2004) 5639-5649
6. Milne T.A., Hughes C.M., Lloyd R., Yang Z., Rozenblatt-Rosen O., Dou Y., et al. Menin and MLL cooperatively regulate expression of cyclin-dependent kinase inhibitors. Proc Natl Acad Sci USA 102 3 (2005) 749-754
7. Dou Y., Milne T.A., Ruthenburg A.J., Lee S., Lee J.W., Verdine G.L., et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 13 8 (2006) 713-719
8. Guenther M.G., Jenner R.G., Chevalier B., Nakamura T., Croce C.M., Canaani E., et al. Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci USA 102 (2005) 8603-8608
9. Caslini C., Serna A., Rossi V., Introna M., and Biondi A. Modulation of cell cycle by graded expression of MLL-AF4 fusion oncoprotein. Leukemia 18 6 (2004) 1064-1071
10. Xia Z.B., Popovic R., Chen J., Theisler C., Stuart T., Santillan D.A., et al. The MLL fusion gene, MLL-AF4, regulates cyclin-dependent kinase inhibitor CDKN1B (p27kip1) expression. Proc Natl Acad Sci USA 102 39 (2005) 14028-14033
11. Gaussmann A., Wenger T., Eberle I., Bursen A., Bracharz S., Herr I., et al. Combined effects of the two reciprocal t(4;11) fusion proteins MLL.AF4 and AF4.MLL confer resistance to apoptosis, cell cycling capacity and growth transformation. Oncogene 26 (2007) 3352-3363
12. Wiederschain D., Kawai H., Shilatifard A., and Yuan Z.M. Multiple mixed lineage leukemia (MLL) fusion proteins suppress p53-mediated response to DNA damage. J Biol Chem 280 26 (2005) 24315-24321
13. Armstrong S.A., Staunton J.E., Silverman L.B., Pieters R., den Boer M.L., Minden M.D., et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 30 1 (2002) 41-47
14. Milne T.A., Dou Y., Martin M.E., Brock H.W., Roeder R.G., and Hess J.L. MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci USA 102 41 (2005) 14765-14770
15. Dell'orto M.C., Banellli B., Giarin E., Accordi B., Trentin L., Romani M., et al. Down-regulation of DLX3 expression in MLL-AF4 childhood lymphoblastic leukemias is mediated by promoter region hypermethylation. Oncol Rep 18 2 (2007) 417-423
16. Nakanishi H., Nakamura T., Canaani E., and Croce C.M. ALL1 fusion proteins induce deregulation of EphA7 and ERK phosphorylation in human acute leukemias. Proc Natl Acad Sci USA 104 36 (2007) 14442-14447
17. Nilson I., Reichel M., Ennas M.G., Greim R., Knörr C., Siegler G., et al. Exon/intron structure of the human AF-4 gene, a member of the AF-4/LAF-4/FMR-2 gene family coding for a nuclear protein with structural alterations in acute leukaemia. Br J Haematol 98 (1997) 157-169
18. Isaacs A.M., Oliver P.L., Jones E.L., Jeans A., Potter A., Hovik B.H., et al. A mutation in Af4 is predicted to cause cerebellar ataxia and cataracts in the robotic mouse. J Neurosci 23 5 (2003) 1631-1637
19. Isnard P., Core N., Naquet P., and Djabali M. Altered lymphoid development in mice deficient for the mAF4 proto-oncogene. Blood 96 2 (2000) 705-710
20. Bitoun E., Oliver P.L., and Davies K.E. The mixed-lineage leukemia fusion partner AF4 stimulates RNA polymerase II transcriptional elongation and mediates coordinated chromatin remodeling. Hum Mol Genet 16 1 (2007) 92-106
21. Mueller D., Bach C., Zeisig D., Garcia-Cuellar M.P., Monroe S., Sreekumar A., et al. A role for the MLL fusion partner ENL in transcriptional elongation and chromatin modification. Blood 110 13 (2007) 4445-4454
22. Erfurth F., Hemenway C.S., de Erkenez A.C., and Domer P.H. MLL fusion partners AF4 and AF9 interact at subnuclear foci. Leukemia 18 1 (2004) 92-102
23. Srinivasan R.S., Nesbit J.B., Marrero L., Erfurth F., LaRussa V.F., and Hemenway C.S. The synthetic peptide PFWT disrupts AF4-AF9 protein complexes and induces apoptosis in t(4;11) leukemia cells. Leukemia 18 8 (2004) 1364-1372
24. Palermo C.M., Bennett C.A., Winters A.C., and Hemenway C.S. The AF4-mimetic peptide, PFWT, induces necrotic cell death in MV4-11 leukemia cells. Leukemia Res 32 4 (2008) 633-642
25. Montecucco A., and Biamonti G. Cellular response to etoposide treatment. Cancer Lett 252 1 (2007) 9-18
26. Cole N., and Gibson B.E. High-dose cytosine arabinoside in the treatment of acute myeloid leukemia. Blood Rev 11 (1997) 39-45
27. Tsutsumi S., and Neckers L. Extracellular heat shock protein 90: a role for a molecular chaperone in cell motility and cancer metastasis. Cancer Sci 98 10 (2007) 1536-1539
28. Patch R.J., Baumann C.A., Liu J., Gibbs A.C., Ott H., Lattanze J., et al. Identification of 2-acylaminothiophene-3-carboxamides as potent inhibitors of FLT3. Bioorg Med Chem Lett 16 12 (2006) 3282-3286
29. Chou T.C., and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22 (1984) 27-55
30. Chou T.-C., and Talalay P. Generalized equations for the analysis of inhibitions of Michaelis-Menten and higher-order kinetic systems with two or more mutually exclusive and nonexclusive inhibitors. Eur J Biochem 115 1 (1981) 207-216
31. Drexler H.G., Quentmeier H., and MacLeod R.A. Malignant hematopoietic cell lines: in vitro models for the study of MLL gene alterations. Leukemia 18 2 (2004) 227-232
32. Potter A.J., and Rabinovitch P.S. The cell cycle phases of DNA damage and repair initiated by topoisomerase II-targeting chemotherapeutic drugs. Mutat Res/Fundam Mol Mech Mutagen 572 1-2 (2005) 27-44
33. Hamada A., Kawaguchi T., and Nakano M. Clinical pharmacokinetics of cytarabine formulations. Clin Pharmacokinet 41 10 (2002) 705-718
34. Zeleznik-Le N.J., Harden A.M., and Rowley J.D. 11q23 translocations split the "AT-hook" cruciform DNA-binding region and the transcriptional repression domain from the activation domain of the mixed-lineage leukemia (MLL) gene. Proc Natl Acad Sci USA 91 22 (1994) 10610-10614
35. Knapper S. FLT3 inhibition in acute myeloid leukaemia. Br J Haematol 138 6 (2007) 687-699
36. Ramanathan R.K., Trump D.L., Eiseman J.L., Belani C.P., Agarwala S.S., Zuhowski E.G., et al. Phase I pharmacokinetic-pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin (17AAG, NSC 330507), a novel inhibitor of heat shock protein 90, in patients with refractory advanced cancers. Clin Cancer Res 11 9 (2005) 3385-3391
37. Banerji U., O'Donnell A., Scurr M., Pacey S., Stapleton S., Asad Y., et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 23 18 (2005) 4152-4161
38. DeAngelo D.J., Stone R.M., Heaney M.L., Nimer S.D., Paquette R.L., Klisovic R.B., et al. Phase 1 clinical results with tandutinib (MLN518), a novel FLT3 antagonist, in patients with acute myelogenous leukemia or high-risk myelodysplastic syndrome: safety, pharmacokinetics, and pharmacodynamics. Blood 108 12 (2006) 3674-3681
39. Knapper S., Burnett A.K., Littlewood T., Kell W.J., Agrawal S., Chopra R., et al. A phase 2 trial of the FLT3 inhibitor lestaurtinib (CEP701) as first-line treatment for older patients with acute myeloid leukemia not considered fit for intensive chemotherapy. Blood 108 10 (2006) 3262-3270
40. Yeoh E.J., Ross M.E., Shurtleff S.A., Williams W.K., Patel D., Mahfouz R., et al. Classification, subtype discovery, and prediction of outcome in pediatric acute lymphoblastic leukemia by gene expression profiling. Cancer Cell 1 2 (2002) 133-143
41. Levis M., Pham R., Smith B.D., and Small D. In vitro studies of a FLT3 inhibitor combined with chemotherapy: sequence of administration is important to achieve synergistic cytotoxic effects. Blood 104 4 (2004) 1145-1150
42. Yao Q., Nishiuchi R., Kitamura T., and Kersey J.H. Human leukemias with mutated FLT3 kinase are synergistically sensitive to FLT3 and Hsp90 inhibitors: the key role of the STAT5 signal transduction pathway. Leukemia 19 9 (2005) 1605-1612
43. Yao Q., Weigel B., and Kersey J. Synergism between etoposide and 17AAG in leukemia cells: critical roles for Hsp90, FLT3, topoisomerase II, Chk1, and Rad51. Clin Cancer Res 13 5 (2007) 1591-1600
44. Yao Q., Nishiuchi R., Li Q., Kumar A.R., Hudson W.A., and Kersey J.H. FLT3 expressing leukemias are selectively sensitive to inhibitors of the molecular chaperone heat shock protein 90 through destabilization of signal transduction-associated kinases. Clin Cancer Res 9 12 (2003) 4483-4493
45. Grant S. Ara-C: cellular and molecular pharmacology. Adv Cancer Res 72 (1998) 197-233
46. Armstrong S.A., Kung A.L., Mabon M.E., Silverman L.B., Stam R.W., Den Boer M.L., et al. Inhibition of FLT3 in MLL. Validation of a therapeutic target identified by gene expression based classification. Cancer Cell 3 2 (2003) 173-183
47. Odgerel T., Kikuchi J., Wada T., Shimizu R., Futaki K., Kano Y., et al. The FLT3 inhibitor PKC412 exerts differential cell cycle effects on leukemic cells depending on the presence of FLT3 mutations. Oncogene 27 22 (2008) 3102-3110
48. Wiederschain D., Kawai H., Gu J., Shilatifard A., and Yuan Z.M. Molecular basis of p53 functional inactivation by the leukemic protein MLL-ELL. Mol Cell Biol 23 12 (2003) 4230-4246
49. Hotfilder M., Rottgers S., Rosemann A., Schrauder A., Schrappe M., Pieters R., et al. Leukemic stem cells in childhood high-risk ALL/t(9;22) and t(4;11) are present in primitive lymphoid-restricted CD34 + CD19-cells. Cancer Res 65 4 (2005) 1442-1449
50. Greaves M. A natural history for pediatric acute leukemia. Blood 82 4 (1993) 1043-1051