Bortezomib-induced sensitization of malignant human glioma cells to vorinostat-induced apoptosis depends on reactive oxygen species production, mitochondrial dysfunction, Noxa upregulation, Mcl-1 cleavage, and DNA damage

Molecular Carcinogenesis

Volumn 52, Issue 2, 2013, Pages 118-133

  Premkumar, Daniel R ^a,b   Jane, Esther P ^a,b   Agostino, Naomi R ^a,b   Didomenico, Joseph D ^b   Pollack, Ian F ^a,b,c  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Apoptosis; Bortezomib; Glioma; Synergy; Vorinostat

Indexed keywords

BORTEZOMIB; CYTOCHROME C; HISTONE H2AX; PROTEIN MCL 1; RAD51 PROTEIN; REACTIVE OXYGEN METABOLITE; VORINOSTAT;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER PATIENT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DOWN REGULATION; DRUG POTENTIATION; GLIOMA; HUMAN; HUMAN CELL; MULTIPLE MYELOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; UPREGULATION;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BORONIC ACIDS; CELL LINE, TUMOR; CENTRAL NERVOUS SYSTEM NEOPLASMS; CYTOCHROMES C; DNA DAMAGE; GLIOBLASTOMA; GLIOMA; HISTONES; HUMANS; HYDROXAMIC ACIDS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MITOCHONDRIA; PHOSPHORYLATION; PROTEASOME INHIBITORS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRAZINES; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED;

EID: 84872601365     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.21835     Document Type: Article

References (57)

1. Omuro AM, Faivre S, Raymond E. Lessons learned in the development of targeted therapy for malignant gliomas. Mol Cancer Ther 2007; 6: 1909-1919.
2. Wolffe AP, Guschin D. Review: Chromatin structural features and targets that regulate transcription. J Struct Biol 2000; 129: 102-122.
3. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK. Histone deacetylases and cancer: Causes and therapies. Nat Rev Cancer 2001; 1: 194-202.
4. Ruefli AA, Ausserlechner MJ, Bernhard D, et al. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci USA 2001; 98: 10833-10838.
5. Burgess A, Ruefli A, Beamish H, et al. Histone deacetylase inhibitors specifically kill nonproliferating tumour cells. Oncogene 2004; 23: 6693-6701.
6. Rao R, Fiskus W, Yang Y, et al. HDAC6 inhibition enhances 17-AAG-mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood 2008; 112: 1886-1893.
7. Marks PA, Breslow R. Dimethyl sulfoxide to vorinostat: Development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 2007; 25: 84-90.
8. Lucas DM, Davis ME, Parthun MR, et al. The histone deacetylase inhibitor MS-275 induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia cells. Leukemia 2004; 18: 1207-1214.
9. Finnin MS, Donigian JR, Cohen A, et al. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 1999; 401: 188-193.
10. Jane EP, Premkumar DR, Addo-Yobo SO, Pollack IF. Abrogation of mitogen-activated protein kinase and Akt signaling by vandetanib synergistically potentiates histone deacetylase inhibitor-induced apoptosis in human glioma cells. J Pharmacol Exp Ther 2009; 331: 327-337.
11. Wetzel M, Premkumar DR, Arnold B, Pollack IF. Effect of trichostatin A, a histone deacetylase inhibitor, on glioma proliferation in vitro by inducing cell cycle arrest and apoptosis. J Neurosurg 2005; 103: 549-556.
12. Yin D, Ong JM, Hu J, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: Effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 2007; 13: 1045-1052.
13. Ugur HC, Ramakrishna N, Bello L, et al. Continuous intracranial administration of suberoylanilide hydroxamic acid (SAHA) inhibits tumor growth in an orthotopic glioma model. J Neurooncol 2007; 83: 267-275.
14. Adams J. The proteasome: A suitable antineoplastic target. Nat Rev Cancer 2004; 4: 349-360.
15. Richardson PG, Barlogie B, Berenson J, et al. Clinical factors predictive of outcome with bortezomib in patients with relapsed, refractory multiple myeloma. Blood 2005; 106: 2977-2981.
16. Jane EP, Premkumar DR, Pollack IF. Bortezomib sensitizes malignant human glioma cells to TRAIL, mediated by inhibition of the NF-{kappa}B signaling pathway. Mol Cancer Ther 2011; 10: 198-208.
17. Aghajanian C, Soignet S, Dizon DS, et al. A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res 2002; 8: 2505-2511.
18. Papandreou CN, Daliani DD, Nix D, et al. Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. J Clin Oncol 2004; 22: 2108-2121.
19. Marcus AI, Zhou J, O'Brate A, et al. The synergistic combination of the farnesyl transferase inhibitor lonafarnib and paclitaxel enhances tubulin acetylation and requires a functional tubulin deacetylase. Cancer Res 2005; 65: 3883-3893.
20. Riss TL, Moravec RA. Comparison of MTT, XTT and a novel tetrazolium compound MTS for in vitro proliferation and chemosensitivity assays. Mol Biol Cell 1992; 3: 184.
21. Jane EP, Premkumar DR, Pollack IF. AG490 influences UCN-01-induced cytotoxicity in glioma cells in a p53-dependent fashion, correlating with effects on BAX cleavage and BAD phosphorylation. Cancer Lett 2007; 257: 36-46.
22. Nencioni A, Wille L, Dal Bello G, et al. Cooperative cytotoxicity of proteasome inhibitors and tumor necrosis factor-related apoptosis-inducing ligand in chemoresistant Bcl-2-overexpressing cells. Clin Cancer Res 2005; 11: 4259-4265.
23. Nagy K, Szekely-Szuts K, Izeradjene K, et al. Proteasome inhibitors sensitize colon carcinoma cells to TRAIL-induced apoptosis via enhanced release of Smac/DIABLO from the mitochondria. Pathol Oncol Res 2006; 12: 133-142.
24. Cossarizza A, Ferraresi R, Troiano L, et al. Simultaneous analysis of reactive oxygen species and reduced glutathione content in living cells by polychromatic flow cytometry. Nat Protoc 2009; 4: 1790-1797.
25. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984; 22: 27-55.
26. Giuliano M, Lauricella M, Calvaruso G, et al. The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res 1999; 59: 5586-5595.
27. 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: 3839-3852.
28. Heider U, von Metzler I, Kaiser M, et al. Synergistic interaction of the histone deacetylase inhibitor SAHA with the proteasome inhibitor bortezomib in mantle cell lymphoma. Eur J Haematol 2008; 80: 133-142.
29. Rosato RR, Almenara JA, Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1 1. Cancer Res 2003; 63: 3637-3645.
30. Miller CP, Ban K, Dujka ME, et al. NPI-0052, a novel proteasome inhibitor, induces caspase-8 and ROS-dependent apoptosis alone and in combination with HDAC inhibitors in leukemia cells. Blood 2007; 110: 267-277.
31. Zheng Y, Yamaguchi H, Tian C, et al. Arsenic trioxide (As(2)O(3)) induces apoptosis through activation of Bax in hematopoietic cells. Oncogene 2005; 24: 3339-3347.
32. Ling YH, Lin R, Perez-Soler R. Erlotinib induces mitochondrial-mediated apoptosis in human H3255 non-small-cell lung cancer cells with epidermal growth factor receptorL858R mutation through mitochondrial oxidative phosphorylation-dependent activation of BAX and BAK. Mol Pharmacol 2008; 74: 793-806.
33. Premkumar DR, Jane EP, Pollack IF. Co-administration of NVP-AEW541 and dasatinib induces mitochondrial-mediated apoptosis through Bax activation in malignant human glioma cell lines. Int J Oncol 2010; 37: 633-643.
34. George NM, Evans JJ, Luo X. A three-helix homo-oligomerization domain containing BH3 and BH1 is responsible for the apoptotic activity of Bax. Genes Dev 2007; 21: 1937-1948.
35. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell 1997; 91: 627-637.
36. Marzo I, Susin SA, Petit PX, et al. Caspases disrupt mitochondrial membrane barrier function. FEBS Lett 1998; 427: 198-202.
37. Lalier L, Cartron PF, Juin P, et al. Bax activation and mitochondrial insertion during apoptosis. Apoptosis 2007; 12: 887-896.
38. Chen L, Willis SN, Wei A, et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 2005; 17: 393-403.
39. Willis SN, Chen L, Dewson G, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005; 19: 1294-1305.
40. Golding SE, Rosenberg E, Khalil A, et al. Double strand break repair by homologous recombination is regulated by cell cycle-independent signaling via ATM in human glioma cells. J Biol Chem 2004; 279: 15402-15410.
41. Ohnishi T, Taki T, Hiraga S, Arita N, Morita T. In vitro and in vivo potentiation of radiosensitivity of malignant gliomas by antisense inhibition of the RAD51 gene. Biochem Biophys Res Commun 1998; 245: 319-324.
42. Russell JS, Brady K, Burgan WE, et al. Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity. Cancer Res 2003; 63: 7377-7383.
43. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 2005; 62: 223-229.
44. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273: 5858-5868.
45. Al-Janadi A, Chandana SR, Conley BA. Histone deacetylation: An attractive target for cancer therapy? Drugs R D 2008; 9: 369-383.
46. Galanis E, Jaeckle KA, Maurer MJ, et al. Phase II trial of vorinostat in recurrent glioblastoma multiforme: A north central cancer treatment group study. J Clin Oncol 2009; 27: 2052-2058.
47. Thaker NG, Zhang F, McDonald PR, et al. Identification of survival genes in human glioblastoma cells by small interfering RNA screening. Mol Pharmacol 2009; 76: 1246-1255.
48. Weller M, Rieger J, Grimmel C, et al. Predicting chemoresistance in human malignant glioma cells: The role of molecular genetic analyses. Int J Cancer 1998; 79: 640-644.
49. Sanchez Y, Simon GP, Calvino E, de Blas E, Aller P. Curcumin stimulates reactive oxygen species production and potentiates apoptosis induction by the antitumor drugs arsenic trioxide and lonidamine in human myeloid leukemia cell lines. J Pharmacol Exp Ther 2010; 335: 114-123.
50. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002; 2: 183-192.
51. Inoue S, Riley J, Gant TW, Dyer MJ, Cohen GM. Apoptosis induced by histone deacetylase inhibitors in leukemic cells is mediated by Bim and Noxa. Leukemia 2007; 21: 1773-1782.
52. Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E, Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 2006; 107: 257-264.
53. Gomez-Bougie P, Wuilleme-Toumi S, Menoret E, et al. Noxa up-regulation and Mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res 2007; 67: 5418-5424.
54. Green DR. At the gates of death. Cancer Cell 2006; 9: 328-330.
55. Kuwana T, Bouchier-Hayes L, Chipuk JE, et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 2005; 17: 525-535.
56. Willis SN, Fletcher JI, Kaufmann T, et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007; 315: 856-859.
57. Han J, Goldstein LA, Gastman BR, Rabinovitz A, Rabinowich H. Disruption of Mcl-1.Bim complex in granzyme B-mediated mitochondrial apoptosis. J Biol Chem 2005; 280: 16383-16392.