Synergistic activity of bortezomib and HDACi in preclinical models of B-cell precursor acute lymphoblastic leukemia via modulation of p53, PI3K/AKT, and NF-κB

Clinical Cancer Research

Volumn 19, Issue 6, 2013, Pages 1445-1457

  Bastian, Lorenz ^a   Hof, Jana ^a   Pfau, Madlen ^a   Fichtner, Iduna ^b   Eckert, Cornelia ^a   Henze, Günter ^a   Prada, Javier ^a   Von Stackelberg, Arend ^a   Seeger, Karl ^a   Shalapour, Shabnam ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASOME; PROTEIN KINASE B; PROTEIN P53; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; UBIQUITIN; VALPROIC ACID;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTILEUKEMIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMIA RELAPSE; MESENCHYME CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROAPOPTOTIC EFFECT; PROTEIN SUBUNIT; STROMA CELL; TUMOR XENOGRAFT; VALIDATION STUDY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BORONIC ACIDS; DRUG SYNERGISM; HISTONE DEACETYLASE INHIBITORS; HUMANS; LEUKEMIA, B-CELL; MICE; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTO-ONCOGENE PROTEINS C-AKT; PYRAZINES; TRANSCRIPTION FACTOR RELA; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84875192633     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-1511     Document Type: Article

References (50)

1. Tallen G, Ratei R, Mann G, Kaspers G, Niggli F, Karachunsky A, et al. Long-term outcome in children with relapsed acute lymphoblastic leukemia after time-point and site-of-relapse stratification and intensified short-course multidrug chemotherapy: results of trial ALL-REZ BFM 90. J Clin Oncol 2010;28:2339-47.
2. Bhatla T, Wang J, Morrison DJ, Raetz EA, Burke MJ, Brown P, et al. Epigenetic reprogramming reverses the relapse-specific gene expression signature and restores chemosensitivity in childhood B-lymphoblastic leukemia. Blood 2012;119:5201-10.
3. Pui CH, Jeha S. New therapeutic strategies for the treatment of acute lymphoblastic leukaemia. Nat Rev Drug Discov 2007;6: 149-65.
4. Einsiedel HG, Kawan L, Eckert C, Witt O, Fichtner I, Henze G, et al. Histone deacetylase inhibitors have antitumor activity in two NOD/SCID mouse models of B-cell precursor childhood acute lymphoblastic leukemia. Leukemia 2006;20:1435-6.
5. Fouladi M, Park JR, Stewart CF, Gilbertson RJ, Schaiquevich P, Sun J, et al. Pediatric phase I trial and pharmacokinetic study of vorinostat: a Children's Oncology Group phase I consortium report. J Clin Oncol 2010;28:3623-9.
6. Su JM, Li XN, Thompson P, Ou CN, Ingle AM, Russell H, et al. Phase 1 study of valproic acid in pediatric patients with refractory solid or CNS tumors: a children's oncology group report. Clin Cancer Res 2011;17: 589-97.
7. Kano Y, Akutsu M, Tsunoda S, Izumi T, Kobayashi H, Mano H, et al. Cytotoxic effects of histone deacetylase inhibitor FK228 (depsipeptide, formally named FR901228) in combination with conventional antileukemia/lymphoma agents against human leukemia/lymphoma cell lines. Invest New Drugs 2007;25:31-40.
8. Bastian L, Einsiedel HG, Henze G, Seeger K, Shalapour S. The sequence of application of methotrexate and histone deacetylase inhibitors determines either a synergistic or an antagonistic response in childhood acute lymphoblastic leukemia cells. Leukemia 2011;25: 359-61.
9. Bhalla S, Balasubramanian S, David K, Sirisawad M, Buggy J, Mauro L, et al. PCI-24781 induces caspase and reactive oxygen speciesdependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin Cancer Res 2009;15: 3354-65.
10. Dai Y, Chen S,Wang L, Pei XY, Kramer LB,Dent P, et al. Bortezomib interacts synergistically with belinostat in human acute myeloid leukaemia and acute lymphoblastic leukaemia cells in association with perturbation in NF-kappaB and Bim. Br J Haematol 2011;153: 222-35.
11. Hideshima T, Bradner JE, Wong J, Chauhan D, Richardson P, Schreiber SL, et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci U S A 2005;102:8567-72.
12. Nawrocki ST, Carew JS, Pino MS, Highshaw RA, Andtbacka RH, Dunner K Jr, et al. Aggresome disruption: a novel strategy to enhance bortezomib-induced apoptosis in pancreatic cancer cells. Cancer Res 2006;66:3773-81.
13. Zhang QL, Wang L, Zhang YW, Jiang XX, Yang F, Wu WL, et al. The proteasome inhibitor bortezomib interacts synergistically with the histone deacetylase inhibitor suberoylanilide hydroxamic acid to induce T-leukemia/lymphoma cells apoptosis. Leukemia 2009;23: 1507-14.
14. Horton TM, Pati D, Plon SE, Thompson PA, Bomgaars LR, Adamson PC, et al. A phase 1 study of the proteasome inhibitor bortezomib in pediatric patients with refractory leukemia: a Children's Oncology Group study. Clin Cancer Res 2007;13:1516-22.
15. Horton TM, Gannavarapu A, Blaney SM, D'Argenio DZ, Plon SE, Berg SL. Bortezomib interactions with chemotherapy agents in acute leukemia in vitro. Cancer Chemother Pharmacol 2006;58:13-23.
16. Pei XY, Dai Y, Grant S. Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors. Clin Cancer Res 2004;10:3839-52.
17. Gerondakis S, Siebenlist U. Roles of the NF-kappaB pathway in lymphocyte development and function. Cold Spring Harb Perspect Biol 2010;2:a000182.
18. Staudt LM. Oncogenic activation of NF-kappaB. Cold Spring Harb Perspect Biol 2010;2:a000109.
19. Derudder E, Cadera EJ, Vahl JC, Wang J, Fox CJ, Zha S, et al. Development of immunoglobulin lambda-chain-positive B cells, but not editing of immunoglobulin kappa-chain, depends on NF-kappaB signals. Nat Immunol 2009;10:647-54.
20. Min DJ, Moskowitz NP, Brownstein C, Lee H, Horton TM, Carroll WL. Diverse pathways mediate chemotherapy-induced cell death in acute lymphoblastic leukemia cell lines. Apoptosis 2006;11:1977-86.
21. Wuchter C, Krappmann D, Cai Z, Ruppert V, Scheidereit C, Dorken B, et al. In vitro susceptibility to TRAIL-induced apoptosis of acute leukemia cells in the context of TRAIL receptor gene expression and constitutive NF-kappa B activity. Leukemia 2001;15:921-8.
22. Weston VJ, Austen B, Wei W, Marston E, Alvi A, Lawson S, et al. Apoptotic resistance to ionizing radiation in pediatric B-precursor acute lymphoblastic leukemia frequently involves increased NF-kappaB survival pathway signaling. Blood 2004;104:1465-73.
23. Rubin EH, Agrawal NG, Friedman EJ, Scott P, Mazina KE, Sun L, et al.A study to determine the effects of food and multiple dosing on the pharmacokinetics of vorinostat given orally to patients with advanced cancer. Clin Cancer Res 2006;12:7039-45.
24. Fichtner I, Paal K, Borgmann A, Badiali L, Wurm R, Henze G. Chemoand radiation sensitivity of xenografted acute lymphoblastic leukemias-correlation to the expression of multidrug resistance proteins. Anticancer Res 2003;23:2657-64.
25. Workman P, Aboagye EO, Balkwill F, Balmain A, Bruder G, Chaplin DJ, et al. Guidelines for the welfare and use of animals in cancer research. Br J Cancer 2010;102:1555-77.
26. Webb JL. Effect of more than one inhibitor. Enzymes and metabolic inhibitors. New York: Academic Press; 1963. p. 66-79 & 487-512.
27. Hof J, Krentz S, van Schewick C, Korner G, Shalapour S, Rhein P, et al. Mutations and deletions of the TP53 gene predict nonresponse to treatment and poor outcome in first relapse of childhood acute lymphoblastic leukemia. J Clin Oncol 2011;29:3185-93.
28. Matsunaga T, Takemoto N, Sato T, Takimoto R, Tanaka I, Fujimi A, et al. Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med 2003;9:1158-65.
29. Shalapour S, Hof J, Kirschner-Schwabe R, Bastian L, Eckert C, Prada J, et al. High VLA-4 expression is associated with adverse outcome and distinct gene expression changes in childhood B-cell precursor acute lymphoblastic leukemia at first relapse. Haematologica 2011; 96:1627-35.
30. Baud V, Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat Rev Drug Discov 2009;8:33-40.
31. Dai Y, Rahmani M, Dent P, Grant S. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-kappaB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol 2005;25:5429-44.
32. Hideshima T, Ikeda H, Chauhan D, Okawa Y, Raje N, Podar K, et al. Bortezomib induces canonical nuclear factor-kappaB activation in multiple myeloma cells. Blood 2009;114:1046-52.
33. Dolcet X, Llobet D, Encinas M, Pallares J, Cabero A, Schoenenberger JA, et al. Proteasome inhibitors induce death but activate NF-kappaB on endometrial carcinoma cell lines and primary culture explants. J Biol Chem 2006;281:22118-30.
34. Wang CY, Cusack JC Jr, Liu R, Baldwin AS Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 1999;5:412-7.
35. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, et al. Control of the senescence-associated secretory phenotype by NFkappaB promotes senescence and enhances chemosensitivity. Genes Dev 2011;25:2125-36.
36. Jing H, Kase J, Dorr JR, Milanovic M, Lenze D, Grau M, et al. Opposing roles of NF-kappaB in anti-cancer treatment outcome unveiled by cross-species investigations. Genes Dev 2011;25:2137-46.
37. Riz I, Zweier-Renn LA, Toma I, Hawley TS, Hawley RG. Apoptotic role of IKK in T-ALL therapeutic response. Mol Cancer Res 2011;9:979-84.
38. Kordes U, Krappmann D, Heissmeyer V, Ludwig WD, Scheidereit C. Transcription factor NF-kappaB is constitutively activated in acute lymphoblastic leukemia cells. Leukemia 2000;14:399-402.
39. Kirschner-Schwabe R, Lottaz C, Todling J, Rhein P, Karawajew L, Eckert C, et al. Expression of late cell cycle genes and an increased proliferative capacity characterize very early relapse of childhood acute lymphoblastic leukemia. Clin Cancer Res 2006;12:4553-61.
40. Shalapour S, Zelmer A, Pfau M,Moderegger E, Costa-Blechschmidt C, van Landeghem FK, et al. The thalidomide analogue, CC-4047, induces apoptosis signaling and growth arrest in childhood acute lymphoblastic leukemia cells in vitro and in vivo. Clin Cancer Res 2006;12:5526-32.
41. Lin KT, Wang YW, Chen CT, Ho CM, Su WH, Jou YS. HDAC inhibitors augmented cell migration and metastasis through induction of PKCs leading to identification of low toxicity modalities for combination cancer therapy. Clin Cancer Res 2012;18:4691-701.
42. Iwamoto S, Mihara K, Downing JR, Pui CH, Campana D. Mesenchymal cells regulate the response of acute lymphoblastic leukemia cells to asparaginase. J Clin Invest 2007;117:1049-57.
43. Befani CD, Vlachostergios PJ, Hatzidaki E, Patrikidou A, Bonanou S, Simos G, et al. Bortezomib represses HIF-1alpha protein expression and nuclear accumulation by inhibiting both PI3K/Akt/TOR and MAPK pathways in prostate cancer cells. J Mol Med (Berl) 2011;90:45-54.
44. Kodani M, Igishi T, Matsumoto S, Chikumi H, Shigeoka Y, Nakanishi H, et al. Suppression of phosphatidylinositol 3-kinase/Akt signaling pathway is a determinant of the sensitivity to a novel histone deacetylase inhibitor, FK228, in lung adenocarcinoma cells. Oncol Rep 2005;13: 477-83.
45. Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int J Biochem Cell Biol 2007;39:1367-74.
46. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009;9:400-14.
47. Wickliffe K, Williamson A, Jin L, Rape M. The multiple layers of ubiquitin-dependent cell cycle control. Chem Rev 2009;109:1537-48.
48. Li J, Lee B, Lee AS. Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 2006;281:7260-70.
49. Perkins ND. The diverse and complex roles of NF-kappaB subunits in cancer. Nat Rev Cancer 2012;12:121-32.
50. Messinger YH, Gaynon PS, Sposto R, van der Giessen J, Eckroth E, Malvar J, et al. Bortezomib with chemotherapy is highly active in advanced B-precursor acute lymphoblastic leukemia: Therapeutic Advances in Childhood Leukemia & Lymphoma (TACL) Study. Blood 2012;120:285-90.